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Impact of adopting a vegan diet or an olestra supplementation on plasma organochlorine concentrations: Results from two pilot studies

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The aim of these studies was to evaluate the potential of some nutritional approaches to prevent or reduce the body load of organochlorines (OC) in humans. Study 1 compared plasma OC concentrations between vegans and omnivores while study 2 verified if the dietary fat substitute olestra could prevent the increase in OC concentrations that is generally observed in response to a weight-reducing programme. In study 1, nine vegans and fifteen omnivores were recruited and the concentrations of twenty-six OC (beta-hexachlorocyclohexane (beta-HCH), p, p'-dichlorodiphenyldichloroethane (p, p'-DDE), p, p'-dichlorodiphenyltrichloroethane (p, p'-DDT), hexachlorobenzene, mirex, aldrin, alpha-chlordane, gamma-chlordane, oxychlordane, cis-nonachlor, trans-nonachlor, polychlorinated biphenyl (PCB) nos. 28, 52, 99, 101, 105, 118, 128, 138, 153, 156, 170, 180, 183 and 187, and aroclor 1260) were determined. In study 2, the concentrations of these twenty-six OC were measured before and after weight loss over 3 months in thirty-seven obese men assigned to one of the following treatments: standard group (33 % fat diet; n 13), fat-reduced group (25 % fat diet; n 14) or fat-substituted group (1/3 of dietary lipids substituted by olestra; n 10). In study 1, plasma concentrations of five OC compounds (aroclor 1260 and PCB 99, PCB 138, PCB 153 and PCB 180) were significantly lower in vegans compared with omnivores. In study 2, beta-HCH was the only OC which decreased in the fat-substituted group while increasing in the other two groups (P = 0.045). In conclusion, there was a trend toward lesser contamination in vegans than in omnivores, and olestra had a favourable influence on beta-HCH but did not prevent plasma hyperconcentration of the other OC during ongoing weight loss.
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Impact of adopting a vegan diet or an olestra supplementation on plasma
organochlorine concentrations: results from two pilot studies
He
´le
`ne Arguin
1
, Marina Sa
´nchez
1
, George A. Bray
2
, Jennifer C. Lovejoy
3
, John C. Peters
4
,
Ronald J. Jandacek
5
, Jean-Philippe Chaput
6
and Angelo Tremblay
1
*
1
Division of Kinesiology, Department of Social and Preventive Medicine, Faculty of Medicine, Laval University, Quebec City,
Quebec, Canada
2
Pennington Biomedical Research Center, Baton Rouge, LA, USA
3
Free and Clear Inc., Seattle, WA, USA
4
Nutrition Science Institute, The Procter & Gamble Company, Cincinnati, OH, USA
5
Department of Pathology and Laboratory Medicine, University of Cincinnati, Cincinnati, OH, USA
6
Department of Human Nutrition, Faculty of Life Sciences, University of Copenhagen, Copenhagen, Denmark
(Received 19 May 2009 – Revised 6 November 2009 – Accepted 9 November 2009 – First published online 24 December 2009)
The aim of these studies was to evaluate the potential of some nutritional approaches to prevent or reduce the body load of organochlorines (OC) in
humans. Study 1 compared plasma OC concentrations between vegans and omnivores while study 2 verified if the dietary fat substitute olestra
could prevent the increase in OC concentrations that is generally observed in response to a weight-reducing programme. In study 1, nine
vegans and fifteen omnivores were recruited and the concentrations of twenty-six OC (b-hexachlorocyclohexane (b-HCH), p,p0-dichlorodiphenyl-
dichloroethane ( p,p0-DDE), p,p0-dichlorodiphenyltrichloroethane ( p,p0-DDT), hexachlorobenzene, mirex, aldrin, a-chlordane, g-chlordane,
oxychlordane, cis-nonachlor, trans-nonachlor, polychlorinated biphenyl (PCB) nos. 28, 52, 99, 101, 105, 118, 128, 138, 153, 156, 170, 180,
183 and 187, and aroclor 1260) were determined. In study 2, the concentrations of these twenty-six OC were measured before and after
weight loss over 3 months in thirty-seven obese men assigned to one of the following treatments: standard group (33 % fat diet; n13), fat-reduced
group (25 % fat diet; n14) or fat-substituted group (1/3 of dietary lipids substituted by olestra; n10). In study 1, plasma concentrations of five OC
compounds (aroclor 1260 and PCB 99, PCB 138, PCB 153 and PCB 180) were significantly lower in vegans compared with omnivores. In study 2,
b-HCH was the only OC which decreased in the fat-substituted group while increasing in the other two groups (P¼0·045). In conclusion, there was
a trend toward lesser contamination in vegans than in omnivores, and olestra had a favourable influence on b-HCH but did not prevent plasma
hyperconcentration of the other OC during ongoing weight loss.
Body fat: Pesticides: Pollutants: Restrictive diets
Organochlorines (OC) are chemical products that were widely
used after World War II as insecticides and in industry. In the
1960s, their adverse effects for the environment and human
health began to be known, and in the 1970s their use was
banned in most industrialised countries. However, because
they are resistant to degradation, many persistent organic
pollutants continue to be present in most food chains
worldwide
(1)
. Furthermore, because of their lipophilicity, OC
accumulate in adipose tissue of organisms. Being at the top
of the food chain, man is contaminated via food, in the infancy
from breast milk
(2)
and later from animal products such as
fish, meat and dairy products
(3,4)
.
The dietary consumption of meat and other animal products
differs among individuals. Diet may vary according to
religion, because of particular health problems or for ecologi-
cal beliefs. Among individuals adhering to different dietary
patterns, vegetarians may be defined as individuals who do
not eat meat. However, among self-defined vegetarians,
some exclude only red meat, while others do not eat any
flesh food, including fish or poultry
(5,6)
. Some vegetarians do
not eat any animal products, including dairy products, eggs
and honey, and are defined as vegans
(6)
. As vegans do not
eat any animal products which are the main source of OC
for man, their exposure to these compounds is theoretically
lower than that of non-vegetarians. Accordingly, some studies
have already shown that OC concentration is lower in
breast milk or in the adipose tissue of vegetarians than in
omnivores
(7 – 9)
. However, to our knowledge, the differences
in plasma OC concentration have not been studied yet between
real vegans and omnivores. It can thus be hypothesised
that vegans would have a lower plasma OC concentration
than omnivores.
*Corresponding author: Dr Angelo Tremblay, fax þ1 418 656 3044, email angelo.tremblay@kin.msp.ulaval.ca
Abbreviations: fT
4
, free thyroxine; b-HCH, b-hexachlorocyclohexane; OC, organochlorines; PCB, polychlorinated biphenyl; T
3
, triiodothyronine; TCDD,
2,3,7,8-tetrachlorodibenzo-p-dioxin.
British Journal of Nutrition (2010), 103, 1433–1441 doi:10.1017/S000711450999331X
qThe Authors 2009
British Journal of Nutrition
As in vegetarians and omnivores, OC plasma and tissue con-
centrations have been compared in individuals who differed in
their weight status. Hue et al.
(10)
showed that, at steady-state
weight, obese and morbidly obese individuals present similar
plasma concentration of OC to lean subjects. They also demon-
strated that total plasma OC concentration is related to age and
not to BMI
(10)
, supporting the suggestion that adipose tissue
could have a protective role, keeping the lipophilic pollutants
away from the organs
(11)
. However, when obese individuals
engage in a weight-loss programme, the body load of OC
becomes more detectable in response to body fat loss which
favours a significant rise of blood and subcutaneous adipose
tissue concentrations
(11 – 13)
. A recent study showed that
plasma OC concentrations were about 388 % greater in obese
subjects at 1 year after biliopancreatic diversion surgery com-
pared with lean controls
(14)
. The increased concentration of
plasma OC induced by weight loss may have several adverse
consequences on health. In fact, exposure to persistent organic
pollutants suppresses the immune system, thereby increasing
the risk of acquiring several human diseases. They are known
to alter thyroid
(15)
and reproductive function
(16)
in both males
and females and to increase the risk of developing cancer
(17)
,
diabetes
(18 – 20)
, Parkinson’s disease
(21)
, cardiovascular disease
and liver disease
(22)
. Women are at high risk of giving birth to
infants of low birth weight, who are at high lifetime risk for
several diseases
(23)
. In addition, the increase in plasma OC
concentrations can induce thermogenic adaptations promoting
weight regain after a weight loss. It is indeed associated with
an accentuation of the decrease in plasma triiodothyronine
(T
3
) concentrations
(24)
and skeletal muscle oxidative
enzymes
(13)
. Moreover, the main predictor of the enhanced fall
in resting
(24)
and sleeping
(25)
metabolic rate observed after
weight loss was found to be the change in total plasma OC
concentration. It is thus clear that the adverse consequences
produced by OC pollutants may aggravate health and the
obesity epidemic.
Up to now, the ingestion of a non-absorbable dietary fat
substitute is the only strategy that has been shown to acceler-
ate the body clearance of OC or analogous compounds
(26)
.
In two individuals acutely contaminated with 2,3,7,8-tetra-
chlorodibenzo-p-dioxin (TCDD), the intake of olestra-contain-
ing potato chips accelerated by 8- to 10-fold the clearance of
TCDD
(27)
. Furthermore, over 2 years of an olestra-containing
diet (20 g/d) leading to a weight loss of 18 kg, the OC aroclor
1254 in the adipose tissue of an obese diabetic male dramati-
cally decreased from 3200 mg/kg to 56 mg/kg
(28)
. This is
concordant with two recent studies reporting that olestra
induced a significant faecal loss of hexachlorobenzene in pre-
contaminated animals
(29)
and that sucrose polyester enhanced
disposal of 2,20,4,40tetrabromodiphenyl ether in rats through
interruption of enteropathic circulation
(30)
. However, since
these observations were made in animal models or in a context
of severe human contamination, uncertainty exists as to what
extent olestra could reduce the level of OC in obese individ-
uals exposed to habitual weight-loss programmes inducing a
small to moderate decrease in the lipid dilution space for OC.
Hence, the main aim of study 1 was to compare plasma OC
concentrations between vegans and omnivores. In addition, the
objective of study 2 was to verify whether olestra can prevent
the increase in plasma OC concentration that is generally
observed in response to a weight-loss programme. The main
preoccupation underlying these two pilot studies was to
evaluate the potential of some nutritional approaches to
prevent or reduce the body load of OC in humans.
Experimental methods
Study 1
Nine vegan subjects (six women and three men) aged 28 72
years participated in the present study. To be eligible for the
study, vegans had to have followed a vegan diet for at least
4 years. Of the nine vegans who participated in the study,
three were also crudivores, i.e. they ate only raw food or
food baked at a maximal temperature of 438C. Their main
food sources were fruits and vegetables, raw nuts and germi-
nated grains. Fifteen omnivores (eleven women and four men)
aged 24–68 years also participated in the study. All subjects
had to be free of any disease that could affect the studied
variables. The present study was conducted according to
the guidelines laid down in the Declaration of Helsinki and
all procedures involving human subjects were approved by
the Laval University Ethics Committee. Written informed
consent was obtained from all subjects.
Body weight and height were measured according
to standardised procedures recommended at the Airlie
Conference
(31)
. BMI was calculated as body weight divided
by height squared (kg/m
2
). To determine body fat mass,
body density was first measured by the hydrostatic weighing
technique. The equation of Siri
(32)
was then used to derive
the percentage of body fat from density. The pulmonary
residual volume required for this calculation was measured
by the He dilution technique
(33)
. The percentage of body fat
was multiplied by body weight to obtain body fat mass;
fat-free mass was then calculated as the difference between
body weight and body fat mass.
RMR was determined by indirect calorimetry after an over-
night fast. Following a 15 min resting period, expired gases
were collected through a mouthpiece for 15 min while the
subject had his nose clipped. A non-dispersive IR analyser
(Uras 10 E; Hartmann & Braun, Frankfurt, Germany) was
used to measure the O
2
and CO
2
concentrations. The pulmonary
ventilation was determined with a S-430A measurement system
(KL Engineering, Ventura, CA, USA). The energy equivalent
of O
2
volume was calculated by the Weir formula
(34)
.
Serum total T
3
and free thyroxine (fT
4
) concentrations were
determined by heterogeneous competitive immunoassay
(Bayer Immuno 1eSystem; Bayer Corp., Tarrytown, NY,
USA). Detection limits were 0·09 nmol/l and 1·3 pmol/l for
T
3
and fT
4
, respectively.
The concentrations of eleven chlorinated pesticides
(b-hexachlorocyclohexane (b-HCH), p,p0-dichlorodiphenyldi-
chloroethane ( p,p0-DDE), p,p0-dichlorodiphenyltrichloroethane
(p,p0-DDT), hexachlorobenzene, mirex, aldrin, a-chlordane,
g-chlordane, oxychlordane, cis-nonachlor, trans-nonachlor),
fourteen polychlorinated biphenyls (PCB), i.e. congeners
with International Union of Pure and Applied Chemistry
(IUPAC) nos. 28, 52, 99, 101, 105, 118, 128, 138, 153, 156,
170, 180, 183 and 187, and one commercial mixture of
PCB (aroclor 1260) were determined in plasma at the
Quebec Toxicological Center. Blood samples were centrifuged
to extract plasma (2 ml) which was then cleaned up on
H. Arguin et al.1434
British Journal of Nutrition
deactivated Florisil columns. Samples were eluted with
methylene chloride–hexane (25:75, v/v) and concentrated to
a final volume of 100 ml. Samples were then analysed on an
HP-5890 series II gas chromatograph with dual-capillary col-
umns and dual
63
Ni electron detectors. Peaks were identified
by their relative retention times obtained on the two columns
using a computer program developed by the Quebec Toxico-
logical Center. Total and free cholesterol (TC and FC),
TAG and phospholipid (PL) plasma concentrations were also
determined by enzymic methods on a Technicon automatic
analyser (RA-500; Bayer Corp.) with test packs. Plasma
total lipids were then calculated with the following summation
method: total lipids ¼1·677ðTC 2FCÞþFC þTAG þPL
(35)
.
Depending on the lipid content, detection limits varied from
0·02 to 0·3 mg/l. The OC concentrations are expressed in
mg/l of plasma and in mg/kg of blood lipids to correct for
the differences in total plasma lipids between individuals.
Study 2
For this study, we took advantage of the results obtained
during the first 3 months of a 9-month parallel-arm, controlled
feeding protocol which was named ‘The Ole Study’. Thirty-
seven overweight/obese (BMI 27 –35 kg/m
2
), healthy and
sedentary men, aged 21 –60 years, completed this project
which was performed at the Pennington Biomedical Research
Center (Baton Rouge, LA, USA), according to previously
described procedures
(36)
. As described in the next paragraph,
the subjects were categorised in three groups differing by
the nature of the dietary regimen to which they were exposed.
In addition, this description indicates that one group was
subjected to an olestra supplementation whereas the other
two groups did not consume this supplement.
The Ole Study
(36)
was aimed at evaluating the effect
on body weight, body fat, lipids, glucose and insulin of a
fat-reduced diet and a diet in which dietary fat was replaced
by olestra, which cooks and has the mouth-feel of normal
fats but cannot be digested in the intestine
(37)
. Subjects
were randomly assigned to one of three diets: a standard
diet aimed at maintaining a weight-stable state (33 %
fat; n13), a fat-reduced diet (25 % digestible fat; n14), or a
fat-substituted diet (one-third of dietary fat replaced by olestra
to achieve a diet containing 25 % metabolisable fat; n10).
The energy level of the fat-substituted and the fat-reduced
diets was designed to be 11 % less than what was determined
during the run-in phase. This was accomplished by reducing
the number of unit foods and the basal diet energy level. How-
ever, the subjects were allowed to request additional snack
packs if they felt hungry or reduce the number of unit foods
consumed if they were too full. Subjects in the standard
group lost an unexpected amount of body weight and fat
mass, even if the foods provided were intended to maintain
body weight. Bray et al.
(36)
suggested that this phenomenon
may reflect the fact that even the 33 % fat diet given during
the run-in period provided less energy as fat than the subjects’
pre-study diets, which was estimated to be close to 39 %.
The present study was conducted according to the guidelines
laid down in the Declaration of Helsinki and all procedures
involving human subjects were approved by the Pennington
Institutional Review Board. Written informed consent was
obtained from all subjects.
Body weight and fat mass were measured at baseline and
after 3 months of intervention by dual-energy X-ray absorptio-
metry with a Hologic QDR 2000 absorptiometer (Hologic Inc.,
Waltham, MA, USA). Blood samples were also taken at base-
line and after 3 months of intervention and OC concentrations
were measured as described in study 1. However, because
no weight-stabilisation period was done before blood samples
were taken, we assumed that body concentrations of OC
were not in a state of equilibrium. Porta et al.
(38)
studied
alternative ways of correcting serum concentrations of OC
compounds other than the OC:total lipids ratio in patients
who were in a state of body dis-equilibrium. They suggested
that it is unwarranted to routinely correct OC by total
lipids and offered alternatives such as no correction for total
blood lipids. In light of this evidence, our statistical analyses
were performed with the OC concentrations expressed as
mass of OC per volume of plasma (mg/l).
Statistical analysis
In study 1, Student’s ttest was used to compare the means of
descriptive characteristics between vegans and omnivores.
In addition, the OC concentrations were compared between
the two groups. Student’s ttest was applied when one non-
detectable entry or less was present and Fisher’s exact test
was used when more than one non-detectable entry was pre-
sent. Pvalues were adjusted for age and BMI. Non-detectable
results were given half the detection limit for statistical con-
siderations. Finally, associations between body fat mass and
total OC concentration were assessed for all the participants.
This was also the case for the determination of the relation-
ships between T
3
,fT
4
or age and total OC concentration.
In study 2, one-way ANOVA was used to compare baseline
age, body weight, fat mass and OC concentrations (Pvalues
adjusted for age, body weight and fat mass), as well as
changes in body weight, fat mass and OC concentrations
(Pvalues adjusted for age, Dbody weight and Dfat mass)
after 3 months of intervention. Post hoc t tests were used
to test for differences between each group if an ANOVA
was significant. To further assess differences of changes in
OC concentrations, the two non-olestra diets (standard diet
and fat-reduced diet) were compared with the olestra diet
(fat-substituted diet) using the appropriate contrast statement
with SAS Mixed procedures (Pvalues adjusted for age,
Dbody weight and Dfat mass). Finally, the changes in fat
mass were correlated to the changes in OC concentrations
between the control group (standardþfat-reduced group) and
the fat-substituted group. The slopes and intercepts of the
regression lines were compared between both groups using
SAS GLM procedures. All statistical analyses were performed
with the SAS software version 9.1 (SAS Institute, Inc., Cary,
NC, USA). Data are given as mean values and standard
deviations. Statistical significance was set at P,0·05.
Results
Study 1
Table 1 presents subjects’ characteristics for vegans and
omnivores. Vegan subjects recruited had been practising a
vegan diet for a mean of 10·2 (SD 4·8) years. They tended to
Preventing body burden of organochlorines 1435
British Journal of Nutrition
be older and leaner than omnivores, with a lower body weight,
BMI, percentage body fat and fat mass, but not to a statisti-
cally significant extent.
There were nine OC compounds that were completely
undetectable in each group (aldrin, a-chlordane, g-chlordane,
cis-nonachlor and PCBnos. 52, 101, 105, 128 and 183). Concen-
trations of the seventeen other pollutants were considered for
statistical analyses. With age and BMI taken into account for
potential confounders, the plasma concentration of four OC com-
pounds (expressed in mg/l) was significantly lower in vegans
compared with omnivores (Table 2). Furthermore, PCB 99
(P¼0·033) was the only OC to be less detectable in the vegans
than in the omnivores (see Table 3). However, when values
were expressed in mg/kg blood lipids, a difference was found
for PCB 99 only (P¼0·023; Table 4). Finally, in Table 2, it is
to be noted that the adjusted means for PCB 180 were 20·029
(SD 0·046) and 0·012 (SD 0·034) mg/l for vegans and omnivores,
respectively, and that they were significantly different (P,0·05)
despite the apparent equality of non-adjusted means.
Correlation analyses were performed by combining the
values of the two groups of subjects. A significant positive
association was observed between fat mass and total plasma
OC concentration (r0·37; P,0·05). Age was also positively
correlated with total plasma OC concentration (r0·63;
P,0·01). Besides, plasma T
3
concentration was negatively
related with total plasma OC concentration (r20·48;
P,0·05). However, no significant association was found
between plasma fT
4
and total plasma OC concentration.
Study 2
There were seven OC compounds that were completely
undetectable in both groups (aldrin, a-chlordane, g-chlordane,
and PCB nos. 52, 101, 105 and 128). Concentrations of the
nineteen other pollutants were considered for statistical
analyses. The baseline characteristics (before treatment) of the
subjects are shown in Table 5. Age, body weight and fat mass
were not significantly different between the groups. After
correction for age, body weight and fat mass, plasma OC con-
centrations were not significantly different between the groups.
Table 6 shows the changes in body weight, fat mass and plasma
concentration of detectable pollutants after 3 months of weight-
loss intervention. All groups showed significant reductions in
body weight and fat mass, which were not significantly different
between the groups. One-way ANOVA showed a difference
between the changes in OC concentrations for b-HCH, which
decreased in the fat-substituted group and increased in the
two other groups (P¼0·045). Post hoc t tests demonstrated a
significant difference between the fat-substituted group and
the fat-reduced group (P¼0·017), a borderline difference
between the fat-substituted and the standard groups (P¼0·050),
and no difference between the two non-olestra diets (P¼0·64).
However, the contrast analysis (data not shown) did not
show a significant difference between the two non-olestra diets
and the fat-substituted diet. Indeed, change in mirex concen-
trations (which increased significantly less in the fat-substituted
group than in the two other groups) was the only significant
Table 2. Plasma organochlorine concentrations (mg/l) in study 1
(Mean values and standard deviations)
Vegans (n9) Omnivores (n15)
Mean SD Mean SD Vegans v. omnivores: P
p,p0-DDE 0·617 0·336 0·586 0·260 0·92
HCB 0·040 0·025 0·054 0·020 0·076
Aroclor 1260 0·891 0·646 1·140 0·817 0·024*
PCB 138 0·052 0·040 0·071 0·048 0·025*
PCB 153 0·119 0·090 0·150 0·109 0·020*
PCB 180 0·100 0·085 0·106 0·089 0·031*
p,p0-DDE, p,p0-dichlorodiphenyldichloroethane; HCB, hexachlorobenzene; PCB, polychlorinated biphenyl.
*P,0·05.
† Analysed by Student’s ttest. Pvalues are adjusted for age and BMI.
Table 1. Characteristics of participants involved in study 1
(Mean values and standard deviations)
Vegans (n9) Omnivores (n15)
Mean SD Mean SD Vegans v. omnivores: P
Age (years) 47·56 14·58 40·27 11·71 0·19
Body weight (kg) 59·72 14·02 68·76 15·92 0·18
BMI (kg/m
2
) 22·78 6·19 24·74 4·46 0·39
Percentage body fat 22·56 10·87 24·17 9·45 0·71
Fat mass (kg) 13·92 10·44 16·87 8·95 0·48
Fat-free mass (kg) 44·94 5·19 51·74 12·60 0·089
Total blood lipids (g/l) 4·79 0·78 5·45 1·01 0·11
Total T
3
(nmol/l) 2·61 0·35 2·39 0·49 0·26
fT
4
(pmol/l) 13·00 1·83 14·47 1·55 0·065
RMR (kJ/d) 6108·6 1150·6 6702·8 1460·2 0·32
T
3
, triiodothyronine; fT
4
, free thyroxine.
H. Arguin et al.1436
British Journal of Nutrition
contrast (P¼0·029). However, as stated earlier, the one-way
ANOVA did not demonstrate a significant difference between
the three groups for this compound.
Finally, as complementary analyses, we combined the
standard and fat-reduced data to form a unique control
group. We correlated the changes in fat mass to the changes
in OC concentrations for the control group and the fat-
substituted group. We compared the slopes and intercepts of
the regression equations derived from these relationships and
found that for all OC, the regression lines tend to parallel
each other. However, no significant differences could be
found between either intercepts or slopes.
Discussion
The main preoccupation underlying the present two pilot
studies was to evaluate the potential of some nutritional
approaches (adopting a vegan diet in study 1 and olestra sup-
plementation in study 2) in an attempt to prevent or reduce the
body load of OC in humans. This issue is of great interest
since the increase in circulating OC has been shown to be
associated with metabolic effects whose common feature is
a decrease in thermogenesis
(13,24,25)
. Thus, the metabolic han-
dicap produced by OC pollutants may complicate obesity
management. It is, however, important to underline the fact
that the present results are the outcome of preliminary work
and that due to evident lack of statistical power, they cannot
be generalised to the entire population and should be inter-
preted with caution. Indeed, non-significant results should be
interpreted as trends.
In study 1, after analysing OC concentrations expressed in
mg/l of plasma, we found that vegans were significantly less
polluted than omnivores regarding aroclor 1260 and PCB
99, PCB 138, PCB 153 and PCB 180, with a trend for
Table 3. Detectable and non-detectable (ND) plasma organochlorines (no. of entries) in study 1
Vegans (n9) Omnivores (n15)
ND Detectable ND Detectable Vegans v. omnivores: P
b-HCH 8 1 13 2 1·00
p,p0-DDT 9 0 13 2 0·51
Mirex 8 1 13 2 1·00
Oxychlordane 6 3 4 11 0·092
Trans-nonachlor 4 5 3 12 0·36
PCB 28 9 0 11 4 0·26
PCB 99 7 2 4 11 0·033*
PCB 118 4 5 3 12 0·36
PCB 156 6 3 10 5 1·00
PCB 170 4 5 5 10 0·68
PCB 187 5 4 5 10 0·40
b-HCH, b-hexachlorocyclohexane; p,p0-DDT, p,p0-dichlorodiphenyltrichloroethane; PCB, polychlorinated biphenyl.
*P,0·05.
Analysed by Fisher’s exact test.
Table 4. Plasma organochlorine concentrations (mg/kg blood lipids) in study 1
(Mean values and standard deviations)
Vegans (n9) Omnivores (n15)
Mean SD Mean SD Vegans v. omnivores: P
b-HCH 6·515 3·294 5·720 2·750 0·92
p,p0-DDE 5·364 1·020 5·908 3·054 0·72
p,p0-DDT 128·964 70·782 107·237 39·659 0·33
HCB 8·431 5·016 10·026 3·566 0·38
Mirex 2·630 1·387 2·248 1·057 0·61
Oxychlordane 3·508 2·246 4·275 1·605 0·14
Trans-nonachlor 5·965 3·971 5·910 2·280 0·61
Aroclor 1260 183·269 126·208 201·612 116·157 0·14
PCB 28 2·146 0·408 2·796 1·859 0·13
PCB 99 2·682 1·041 4·891 2·691 0·023*
PCB 118 5·735 5·065 6·838 5·894 0·35
PCB 138 10·685 8·461 12·553 6·770 0·14
PCB 153 24·362 17·285 26·421 15·653 0·12
PCB 156 3·587 2·326 3·099 2·343 0·59
PCB 170 5·894 4·750 5·766 4·828 0·094
PCB 180 20·035 15·572 18·594 13·332 0·17
PCB 187 4·024 2·561 4·060 2·460 0·20
b-HCH, b-hexachlorocyclohexane; p,p0-DDE, p,p0-dichlorodiphenyldichloroethane; p,p0-DDT, p,p0-dichlorodiphenyltrichloroethane; HCB, hexachlorobenzene;
PCB, polychlorinated biphenyl.
*P,0·05.
† Analysed by Student’s ttest. Pvalues are adjusted for age and BMI.
Preventing body burden of organochlorines 1437
British Journal of Nutrition
hexachlorobenzene (P¼0·076) and oxychlordane (P¼0·092),
even after adjustment for age and BMI. These findings are
striking considering the very low power of the study and are
in accordance with previous studies that found a lower OC
concentration in breast milk and adipose tissue of vegetarians
compared with omnivores
(7 – 9)
. Interestingly, when corrected
for serum lipid values, OC concentrations tended to be similar
between both groups (with the exception of PCB 99;
P¼0·023). The latter results are strengthened by Fisher’s
exact test that showed a difference for PCB 99 only
(P¼0·033). In this regard, it is reasonable to hypothesise
that significance could be obtained in other OC concentrations
with larger sample sizes that provide more statistical power.
A certain number of factors may explain why we did not see
a difference in all plasma OC concentrations between vegan
and omnivore subjects. First, studies that found a lower OC
concentration in breast milk and adipose tissue of vegetarians
are all more than 25 years old. In that period, the concen-
trations of OC in humans and animal products were higher.
Now, we are exposed to much lower levels and it might be
that we have reached a steady state. For example, in a
recent study by Agudo et al.
(39)
, the concentration of PCB
in Spanish adults was on average 12 % higher in samples
from 1993 than those from 1995. Second, the vegans in the
present study may have been breast-fed as infants, and
might thus have been exposed to OC accumulated by the
mother and which are transferred to her baby at the time of
lactation
(40,41)
. Moreover, becoming a vegetarian or a vegan
is often a decision that is made in adulthood. Thus, the omni-
vore diet followed during childhood and adolescence results in
a contamination by OC that is still detectable in adults, since
these compounds are resistant to degradation. In order to see a
significant difference between plasma OC concentration in
vegans and omnivores, we should maybe study individuals
that have been vegans for more than 10 years. In fact, PCB
half-lives have been found to be 5–25 years, depending of
the specific congener make-up of the PCB mixture
(42)
.
Another reason that may explain the presence of OC in
vegans is that they were 7 years older than the omnivores.
In our cohort, age was positively correlated with total
plasma OC concentration, suggesting an OC accumulation
with age. This observation is concordant with our recently
reported data
(10,14)
and those published by other investi-
gators
(43 – 48)
. In addition, vegans may, on rare occasions,
depart from their diet and eat some animal products. In
addition, the consumption of imported fruits containing OC
may also be a problem
(49)
. Furthermore, it is relevant to
emphasise that the contamination might not only come from
food sources. Indeed, there are countries that still use OC
which can be transported by air and thus contaminate rivers
and fields of other countries, particularly in Nordic
areas
(50 – 52)
. In this respect, OC may contaminate the water
that vegans drink, the air that they breathe and the vegetables,
fruits and cereals that grow in fields. Therefore, even if an
individual eats exclusively biologically certified food,
exposure to OC is not excluded.
We observed a positive correlation between fat mass and
total plasma OC concentration, and this finding agrees with
many previously reported studies
(11,53)
. Indeed, the body
load of these lipid-soluble compounds is increased in obese
individuals because of their increased dilution space (body
fat mass) and slightly increased concentrations in plasma
Table 5. Baseline characteristics of the participants involved in study 2
(Mean values and standard deviations)
Standard (33 % fat)
(n13)
Fat-reduced
(25 % fat) (n14) Fat-substituted (n10)
Variables Mean SD Mean SD Mean SD Between groups: P
Age (years) 36·84 10·49 37·29 8·71 40·10 7·11 0·66
Body weight (kg) 96·84 10·93 98·34 11·15 100·84 11·61 0·70
Fat mass (kg) 31·49 4·09 31·06 4·14 34·30 7·26 0·29
b-HCH (mg/l) 0·045 0·042 0·051 0·032 0·088 0·079 0·27
p,p0-DDE (mg/l) 1·532 1·493 1·896 1·118 2·650 1·908 0·22
p,p0-DDT (mg/l) 0·025 0·000 0·043 0·060 0·030 0·011 0·39
HCB (mg/l) 0·082 0·060 0·067 0·024 0·081 0·034 0·52
Mirex (mg/l) 0·136 0·190 0·116 0·110 0·135 0·126 0·92
Oxychlordane (mg/l) 0·093 0·068 0·101 0·057 0·117 0·051 0·86
Trans-nonachlor (mg/l) 0·159 0·126 0·179 0·076 0·217 0·103 0·57
Cis-nonachlor (mg/l) 0·018 0·015 0·020 0·010 0·022 0·010 0·82
Aroclor 1260 (mg/l) 1·357 1·065 1·502 0·955 1·650 0·624 0·86
PCB 28 (mg/l) 0·019 0·033 0·010 0·000 0·012 0·004 0·39
PCB 99 (mg/l) 0·026 0·018 0·029 0·016 0·037 0·013 0·31
PCB 118 (mg/l) 0·044 0·044 0·041 0·026 0·052 0·022 0·88
PCB 138 (mg/l) 0·088 0·064 0·099 0·063 0·115 0·042 0·68
PCB 153 (mg/l) 0·173 0·140 0·194 0·125 0·204 0·076 0·83
PCB 156 (mg/l) 0·026 0·020 0·031 0·022 0·027 0·011 0·42
PCB 170 (mg/l) 0·043 0·035 0·046 0·034 0·045 0·022 0·71
PCB 180 (mg/l) 0·139 0·119 0·147 0·106 0·152 0·071 0·90
PCB 183 (mg/l) 0·016 0·008 0·014 0·008 0·016 0·010 0·76
PCB 187 (mg/l) 0·044 0·041 0·042 0·027 0·049 0·024 0·97
b-HCH, b-hexachlorocyclohexane; p,p0-DDE, p,p0-dichlorodiphenyldichloroethane; p,p0-DDT, p,p0-dichlorodiphenyltrichloroethane; HCB, hexachlorobenzene;
PCB, polychlorinated biphenyl.
Pvalues for differences in organochlorine concentrations are adjusted for age, body weight and fat mass.
H. Arguin et al.1438
British Journal of Nutrition
and fat tissues
(24)
. Finally, the fact that plasma T
3
concen-
tration was negatively related with total plasma OC concen-
tration is consistent with the results of Cheek et al.
(54)
who
showed that changes in OC concentrations alter the serum
level of some hormones because they have a thyroid
hormone-like affinity for the serum transport protein trans-
thyretin. Furthermore, recent results from our laboratory
showed that body weight/fat loss is related to a greater than
predicted decrease in plasma T
3
concentration
(24)
.
After severe contamination, the ingestion of olestra is the
only potential solution that has been shown to accelerate the
body clearance of OC
(27 – 29)
. To our knowledge, however,
olestra’s depolluting effects in human have not been investi-
gated with lower levels of contamination that are generally
observed in response to the usual weight-reducing
programmes. Thus, study 2 is the first to examine the extent
to which olestra could prevent the increase in plasma OC
concentrations following a small to moderate decrease in the
lipid dilution space for OC. With the exception of b-HCH,
which decreased in the fat-substituted group while increasing
in the two other groups (P¼0·045), changes in OC concen-
trations were not significantly different between the groups.
Moreover, when the two non-olestra groups are compared
with the fat-substituted group by contrast analyses, only
mirex shows a significant difference (P¼0·029). However,
this result appears to be mainly driven by the standard diet
group giving a high mean value and should be interpreted
with caution since the one-way ANOVA did not demonstrate
a difference between the three groups. These results were
reinforced by the fact that no significant differences were
seen between the slopes and intercepts of the regression
lines correlating changes in fat mass and changes in OC
concentrations. Once again, these results are preliminary and
would necessitate larger sample sizes to really detect an
effect of olestra.
Apart from the small sample sizes, some limitations of the
present study could also contribute to explain the apparent
inability of olestra to reduce most OC plasma concentrations.
First, the range that we have on the body burden of OC
(plasma concentrations) reflects a relatively stable depot (adi-
pose concentrations) that is in equilibrium with the plasma
(29)
.
There is no clear indication about the possible influence of
duration of weight loss on the mobilisation of OC from tissues
to the blood circulation. Thus, in the present study, a 3-month
weight-loss period could have been too short to show a depol-
luting effect. Another possible explanation could be that the
doses of olestra administrated to the participants were too
low to prevent the hyperconcentrations of OC. In fact, a pre-
vious study showing a potential depolluting role for olestra
was based on results derived from experiments in mice,
which received relatively high dosages in terms of human
levels
(29)
. Moreover, human subjects in whom a depolluting
effect of olestra was observed were severely contaminated
with TCDD
(27)
and aroclor 1254
(28)
, which may suggest that
the body load of our subjects was too low to detect an
effect of olestra. Moreover, we based our analyses on changes
in plasma OC concentrations alone but not on changes that
could have resulted in other tissues or by way of faecal
Table 6. Comparison of changes in weight, fat mass and plasma organochlorine concentrations between the standard, the fat-reduced and
the fat-substituted groups in study 2
(Mean values and standard deviations)
Standard (33 % fat)
(n13)
Fat-reduced
(25 % fat) (n14) Fat-substituted (n10)
Variables‡ Mean SD Mean SD Mean SD Between groups: P
DBody weight (kg) 24·63 2·45 23·707 2·547 24·76 3·29 0·57
DFat mass (kg) 22·61 2·06 22·66 1·56 23·65 2·60 0·42
Db-HCH (mg/l) 0·009
a,b
0·019 0·015
b
0·035 20·009
a
0·034 0·045*
Dp,p0-DDE (mg/l) 0·320 0·561 0·345 0·578 0·176 0·752 0·35
Dp,p0-DDT (mg/l) 0·005 0·011 0·005 0·014 0·002 0·013 0·40
DHCB (mg/l) 0·001 0·027 0·015 0·009 0·008 0·010 0·20
DMirex (mg/l) 0·065 0·143 0·024 0·052 0·010 0·050 0·078
DOxychlordane (mg/l) 0·017 0·035 0·026 0·029 0·008 0·031 0·12
DTrans-nonachlor (mg/l) 0·028 0·049 0·044 0·039 0·018 0·067 0·20
DCis-nonachlor (mg/l) 0·001 0·006 0·006 0·006 0·002 0·004 0·074
DAroclor 1260 (mg/l) 0·193 0·554 0·416 0·593 0·118 0·388 0·10
DPCB 28 (mg/l) 0·007 0·025 0·001 0·004 0·003 0·005 0·84
DPCB 99 (mg/l) 0·006 0·011 0·006 0·014 0·001 0·015 0·30
DPCB 118 (mg/l) 0·005 0·010 0·009 0·022 0·002 0·019 0·46
DPCB 138 (mg/l) 0·012 0·042 0·026 0·044 0·006 0·029 0·16
DPCB 153 (mg/l) 0·024 0·070 0·048 0·070 0·017 0·047 0·15
DPCB 156 (mg/l) 0·003 0·012 0·007 0·010 0·003 0·005 0·24
DPCB 170 (mg/l) 0·005 0·018 0·011 0·016 0·007 0·008 0·38
DPCB 180 (mg/l) 0·018 0·050 0·029 0·047 0·017 0·027 0·33
DPCB 183 (mg/l) 0·002 0·008 0·004 0·006 0·003 0·009 0·51
DPCB 187 (mg/l) 0·006 0·014 0·009 0·015 0·005 0·012 0·30
b-HCH, b-hexachlorocyclohexane; p,p0-DDE, p,p0-dichlorodiphenyldichloroethane; p,p0-DDT, p,p0-dichlorodiphenyltrichloroethane; HCB, hexachlorobenzene;
PCB, polychlorinated biphenyl.
a,b
Mean values with unlike superscript letters were significantly different (P¼0·017).
*P,0·05.
Pvalues for differences in Dorganochlorine concentrations are adjusted for age, Dbody weight and Dfat mass.
‡ The deltas (D) are equal to the values after 3 months of treatment minus the values before treatment.
Preventing body burden of organochlorines 1439
British Journal of Nutrition
excretion. In fact, in previous studies, olestra had large effects
on reduction of OC concentrations in tissues
(29,28)
with little
effect on plasma levels. Taken together, these observations
support the relevance of retesting the effects of olestra on
plasma and tissue concentrations and on faecal excretion of
OC in obese patients experiencing a larger weight loss, such
as massively obese patients subjected to bariatric surgery.
For instance, in a recent study, the mean cumulative plasma
concentration of OC was found to increase by 388 % at
1 year after a biliopancreatic diversion
(14)
. In such patients,
olestra might exert a detectable depolluting effect that could
facilitate the control of energy expenditure and eventually
help prevent weight regain. Finally, in the present study,
there was no weight-stabilisation period before blood samples
were taken. Lack of weight stability should have influenced
the results because the plasma and adipose tissue compart-
ments would probably not be in equilibrium. Thus, any
effect of olestra to drain OC via the stool would not show
its full effect in plasma.
In summary, the two pilot studies presented in this paper
represent a valuable effort aiming at evaluating the potential
of some nutritional approaches to prevent or reduce the
body load of OC in humans. Taken together, these obser-
vations emphasise the difficulty of preventing body
accumulation or promoting clearance of OC compounds in
free-living individuals. The first study seems to demonstrate
trends in favour of a preventive effect of a vegan diet.
In study 2, olestra favourably influenced the plasma concen-
trations of b-HCH but the data do not yield enough evidence
to support an effect on the other OC compounds measured
before and after the weight-loss programme. For individuals
subjected to weight loss, studies of greater statistical power
(sample sizes more than twenty individuals) and longer
duration (.3 months) in individuals displaying a greater
body load of pollutants (morbidly obese, older, omnivores
and/or professionally exposed to OC) and given more pro-
nounced doses of a therapeutic agent, for example, olestra,
are necessary before excluding OC clearance as a target of
nutritional decontaminating approaches.
Acknowledgements
The authors express their gratitude to the participants for
their excellent collaboration and the staff members for their
contribution to both studies. They also thank Claude Leblanc
for his important contribution to the statistical analyses.
Study 1 was supported by the Canada Research Chair in
Environment and Energy Balance. The Ole Study (Baton
Rouge) was supported in part by grant 96034323-3031 from
the United States Department of Agriculture and by the
Procter and Gamble Co., Cincinnati. H. A. is supported by
the Fonds de la Recherche en Sante
´du Que
´bec (FRSQ).
H. A. drafted the manuscript and contributed to data
analysis. M. S. contributed to the development of the design
of study 1, tested subjects and contributed to data analysis.
G. A. B. and J. C. L. contributed to the development of the
design of study 2 and to its realisation. J. C. P. contributed
to the preparation of the manuscript, particularly in regards
to the effects of olestra. R. J. J. contributed to the preparation
of the manuscript, particularly about the body clearance of
OC. J.-P. C. contributed to data analysis and to the preparation
of some parts of the manuscript. A. T. contributed to the
development of the design of study 1 and to its realisation.
He also planned the conceptual integration of the global
issue documented in this paper. All authors contributed to
the revision of the manuscript.
There are no conflicts of interest to declare.
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Preventing body burden of organochlorines 1441
British Journal of Nutrition
... Indeed, following a body fat loss of about 3 kg, Olestra accentuated the clearance of β-hexachlorocyclohexane which significantly differed from its increase in blood concentrations following a comparable fat loss without Olestra. However, we did not find significant differences for changes in 18 other pollutants in response to Olestra supplementation (55). ...
... There is also no clear evidence showing that specific dietary modifications can exert a substantial body detoxifying effect. For instance, when comparing blood organochlorine concentrations between omnivores and vegans, only small differences favoring vegans were observed between the two groups (55). Interestingly, a relationship between the concentrations of body pollutants and some gut bacteria was also recently reported (56). ...
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The prevalence of overweight has substantially increased over the last decades despite the intent of health professionals and the general population to prevent this trend. Traditionally, this phenomenon has been attributed to unhealthy dietary macronutrient composition and/or to the decrease in physical activity participation. Beyond the influence of these factors, it is more than likely that other factors have influenced energy balance in a context of modernity. These include inadequate sleep, demanding cognitive effort, chemical pollution, and probably others which also have the potential to promote a positive energy balance but which are also part of the reality of success and productivity in a globalized world. As discussed in this paper, many individuals may become conflicted with themselves if they wish to prevent weight gain while influencing factors which are determinants of their socioeconomic success. In this regard, this paper reminds us of the contribution of adipose tissue gain in body homeostasis which is essential to permit energy balance, especially under lifestyle conditions promoting overfeeding. From a clinical standpoint, this imposes the consideration of a weight loss program as a search for compromise between what can be changed to promote a negative energy balance and what can be tolerated by the body in terms of fat loss. Furthermore, if we also consider the impact of pollution on energy balance for which we currently do not hold solutions of reversibility, we probably must accept that the mankind of today will have to be more corpulent than its ancestors. In this pessimistic environment, there are still possibilities to do better; however, this will probably require the revisiting of lifestyle practices according to what the human body and planet can tolerate as deviation from optimal functioning.
... A summary of HBM studies on α-HCH, β-HCH, and dicofol concentrations published during the last 10 years is shown in Supplementary Material, Table S5. There are still a few HBM studies using adipose tissue [26][27][28][29][30][31][32], breastmilk [51][52][53][54][55][56][57], placenta [58], and meconium [59] as biological matrices to assess the OCPs exposure compared to the number of studies using serum [45][46][47][48], blood [98][99][100][101][102][103][104][105][106], and plasma [5,49,[107][108][109][110][111][112][113][114]. Moreover, two studies used two biological matrices such as serum and placenta [115] or serum and omentum fat [116]. ...
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To identify bioaccumulation patterns of α-, β- hexachlorocyclohexane (HCH) and dicofol in relation to sociodemographic, dietary, and lifestyle factors, adipose tissue samples of 387 subjects from GraMo cohort in Southern Spain were analyzed. Potential predictors of these organochlorine pesticides (OCP) levels were collected by face-to-face interviews and assessed by multivariable linear and logistic regression. OCPs were detected in 84.2% (β-HCH), 21.7% (α-HCH), and 19.6% (dicofol) of the population. β-HCH levels were positively related to age, body mass index (BMI), mother’s occupation in agriculture during pregnancy, living in Poniente and Alpujarras, white fish, milk and water consumption, and negatively related to being male, living near to an agricultural area, working ≥10 years in agriculture, and beer consumption. Detectable α-HCH levels were positively related to age, BMI, milk consumption, mother’s occupation in agriculture during pregnancy, and negatively with residence in Poniente and Alpujarras, Granada city, and Granada Metropolitan Area. Residence near to an agricultural area, smoking habit, white fish and water consumption, and living in Poniente and Alpujarras, Granada city and Granada Metropolitan Area were negatively associated with detectable dicofol levels. Our study revealed different bioaccumulation patterns of α, β-HCH and dicofol, probably due to their dissimilar period of use, and emphasize the need for assessing the exposure to frequently overlooked pollutants.
... Despite the impossibility to completely avoid exposure, certain dietary strategies have shown to decrease exposure levels (Arguin et al., 2010;Guo et al., 2016;Lignell et al., 2016;Perkins et al., 2016;Gupta et al., 2018). Therefore, chronic exposure to OCPs and PCBs could be considered, to some extent, as potentially modifiable. ...
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Background: Despite restrictions on their production and use, most of the population is still exposed to Persistent Organic Pollutants (POPs), including organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs). These chemicals are thought to contribute to the aetiology of highly prevalent chronic conditions, such as cardiovascular diseases (CVDs), although current evidences are still controversial. Objectives: To explore the potential contribution of historical POP exposure to 15-year pharmaceutical consumption in relation to CVD. Methods: This study is framed within GraMo adult cohort. Participants (n = 387) were recruited in two hospitals in Granada province, Southern Spain (2003-2004). Historical exposure to 5 OCPs and 3 non-dioxine-like PCBs was estimated by analysing adipose tissue concentrations at recruitment. Pharmaceutical consumption from recruitment until year 2017 was quantified by reviewing dispensation databases. Average consumption increase (ACI) in CVD medication was calculated by subtracting average consumption in 2002 to the average yearly consumption during follow-up. ACI was expressed as Defined Daily Dose (DDD)/year units. Data analyses were carried out using a multivariable multinomial logistic regression and weighted quantile sum regression (WQS), with ACI categorized in quartiles (Q) as the dependent variable. Results: Concentrations of most pollutants showed a positive trend with the quartiles of ACI. Particularly, PCB-153 showed increasing and statistically significant odds ratios (ORs) for Q2 (OR: 1.27, 95% confidence interval (CI): 1.07-1.52), Q3 (OR: 1.49, 95 %CI: 1.17-1.88) and Q4 (OR: 1.42, 95 %CI: 1.13-1.78) vs Q1. Similarly, beta-hexachlorocyclohexane (β-HCH) also showed increasing ORs, that reached statistical significance in Q4 (OR: 1.36, 95 %CI: 1.06-1.74) vs Q1. These findings were corroborated by WQS analyses, that revealed a significant mixture effect, predominantly accounted for by PCB-153 and β-HCH. Discussion: Our results suggest that long-term POP exposure might represent a modifiable risk factor for CVD. These findings are relevant for public health campaigns and management, since pharmaceutical consumption is considered an indicator of both morbidity and health expenditure.
... However, this point has to be confirmed through longitudinal studies lasting more than 12 months after surgery and including pre-and post-natal period. This delay to pregnancy could be positively used to foster POP elimination by adapting diet (Jandacek et al., 2014;Arguin et al., 2010) with fibers and resin chelators such as cholestyramine (Mochida et al., 2007) which have also been proposed. It gives time for delivering advices to prevent or reduce secondary exposure to exogenous POPs (Fenichel et al., 2016) from domestic environment. ...
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... Sendo assim, indivíduos adeptos da dieta vegetariana estrita que não consomem esses alimentos fortificados apresentam deficiência no consumo da vitamina B12, de acordo com Koebniek et al. (2004). Em um estudo feito por Arguin (2010), em onívoras e vegetarianas norte--americanas e finlandesas, constatou-se que em ambos os grupos, 50% apresentavam deficiência de vitamina B12. Já estudos feitos no Brasil por Almeida et al. (2004) indicam que esses valores ultrapassam os 50%. ...
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