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European Journal of Clinical Nutrition (2011), 1–7
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ORIGINAL ARTICLE
The impact of pistachio intake alone or in
combination with high-carbohydrate foods
on post-prandial glycemia
CWC Kendall1,2,3, AR Josse4, A Esfahani1,2,5 and DJA Jenkins1,2,6
1
Clinical Nutrition and Risk Factor Modification Center, St. Michael’s Hospital, Toronto, Ontario, Canada; 2Department of Nutritional
Sciences, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada; 3College of Pharmacy and Nutrition, University of
Saskatchewan, Saskatoon, Saskatchewan, Canada; 4Department of Kinesiology, McMaster University, Hamilton, Ontario, Canada;
5
School of Medicine, New York Medical College, Valhalla, New York, USA and 6Department of Medicine, Division of Endocrinology and
Metabolism, St Michael’s Hospital, Toronto, Ontario, Canada
Background/Objectives: Dietary strategies that reduce post-prandial glycemia are important in the prevention and treatment
of diabetes and coronary heart disease (CHD). This may be achieved by addition of high-quality protein and fat contained in
pistachio nuts, to carbohydrate-containing foods or meals.
Subjects/Methods: A total of 10 healthy volunteers (3 males, 7 females); aged 48.3±6.4 years; Body mass index (BMI)
28.0±4.8 kg/m2 participated in two studies. Study 1 assessed the dose-response effect of 28, 56 and 84 g pistachios consumed
alone or co-ingested with white bread (50 g available carbohydrate); Study 2 assessed the effective dose (56 g) of pistachios on
post-prandial glycemia consumed with different commonly consumed carbohydrate foods (50 g available carbohydrate).
Relative glycemic responses (RGRs) of study meals compared with white bread, were assessed over the 2 h post-prandial period.
Results: The RGRs of pistachios consumed alone expressed as a percentage of white bread (100%) were: 28 g (5.7±1.8%); 56 g
(3.8±1.8%); 84 g (9.3±3.2%), Po0.001. Adding pistachios to white bread resulted in a dose-dependent reduction in the RGR
of the composite meal; 28 g (89.1±6.0, P ¼ 0.100); 56 g (67.3±9.8, P ¼ 0.009); 84 g (51.5±7.5, Po0.001). Addition of 56 g
pistachios to carbohydrate foods significantly reduced the RGR: parboiled rice (72.5±6.0) versus rice and pistachios (58.7±5.1)
(P ¼ 0.031); pasta (94.8±11.4) versus pasta and pistachios (56.4±5.0) (P ¼ 0.025); whereas for mashed potatoes (109.0±6.6)
versus potatoes and pistachios, (87.4±8.0) (P ¼ 0.063) the results approached significance.
Conclusions: Pistachios consumed alone had a minimal effect on post-prandial glycemia and when taken with a carbohydrate
meal attenuated the RGR. The beneficial effects of pistachios on post-prandial glycemia could, therefore, be part of the
mechanism by which nuts reduce the risk of diabetes and CHD.
European Journal of Clinical Nutrition advance online publication, 2 March 2011; doi:10.1038/ejcn.2011.12
Keywords: pistachios; nuts; glycemic index; glycemic load; diabetes
Introduction
Post-meal hyperglycemia is an independent risk factor for
cardiovascular disease (CVD) (Levitan et al., 2004) and a
condition that is common in patients with type 2 diabetes
(Akbar, 2003; Bonora et al., 2006). Dietary glycemic index
(GI) and glycemic load have been shown to reliably predict the
Correspondence: Dr CWC Kendall, Department of Nutritional Sciences,
Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada,
M5S 3E2.
E-mail: [email protected]
Received 11 August 2010; revised 13 December 2010; accepted 13 January
2011
relative post-meal glycemic and insulinemic responses to
mixed meals (McMillan-Price et al., 2006; Wolever et al.,
2006), and evidence suggests that lowering the GI of a diet can
positively affect post-meal plasma glucose excursions (Opperman et al., 2004) and as such, potentially reduce the risk of
CVD and diabetes (Salmeron et al., 1997a, b; Liu et al., 2000)
Epidemiological and interventional studies have linked
the intake of tree nuts to reduced risk of CVD and diabetes
(Jiang et al., 2002; Li et al., 2009; Mente et al., 2009). This
protective effect may in part be explained by the favorable
impact of nuts on serum lipids (Griel and Kris-Etherton,
2006), oxidative stress (Jenkins et al., 2002) and markers of
inflammation (Jiang et al., 2006; Ros, 2009). However, owing to
their low available carbohydrate content and favorable fat and
Pistachios improve post-prandial glycemia
CWC Kendall et al
2
protein profiles, nuts may also decrease the risk of CVD and
diabetes by reducing post-prandial blood glucose excursions.
This mechanism has only been examined in a few clinical
studies, which have shown that almonds eaten alone have a
minimal effect on blood glucose, and when different doses are
consumed with a carbohydrate meal, the post-prandial glucose
response is attenuated (Josse et al., 2007).
To further test the potential impact of nuts on post-meal
hyperglycemia, we conducted two studies using pistachio
nuts. The first assessed the dose-response effect of pistachios
on post-prandial blood glucose when consumed alone,
and consumed with a white bread meal. The second
study assessed the effect of pistachios on post-prandial
blood glucose excursions when added to other commonly
consumed carbohydrate-rich foods.
week with at least one day in between tests. On each test day,
subjects came to the research clinic in the morning after
a 10–14 h overnight fast. After being weighed and having
a fasting blood sample obtained by finger-prick using
autolancets (Microlet, Bayer, Toronto, Canada), the subject
then consumed a study meal within 10 min, and further
finger-prick blood samples were obtained at 15, 30, 45, 60, 90
and 120 min after the start of the meal. Subjects were given a
choice of one or two cups of water, tea or coffee with or
without milk. The beverage consumed by each subject
remained the same for each of their study days. Subjects
were instructed not to consume nuts the day before each
study day.
The study protocol was approved by the Western
Institutional Review Board. Written informed consent was
obtained from all subjects before the start of the study.
Subjects and methods
Subjects
A total of 10 overweight but otherwise healthy subjects (3
males and 7 females), aged (mean±s.d.) 48.3±6.4 years with
a body mass index of 28.0±4.8 kg/m2, were studied. Subjects
were not taking any medications that would interfere with
glucose metabolism.
Protocol
Subjects were recruited through local advertisement and
through the clinic volunteer roster. Each subject underwent
treatments on separate days, performing up to two tests per
Meals and palatability
The tests meals in study 1 consisted of three different doses
(28, 56 and 84g) of pistachio nuts either consumed alone or
together with white bread (50 g available carbohydrate)
(Table 1). In study 2, 50 g available carbohydrate portions
of rice, pasta or instant mashed potatoes were consumed
with or without 56 g of pistachios (Table 1). The control
white bread was also consumed on three different occasions
to allow calculation of the relative glycemic response (RGR).
The control white bread was baked in a bread maker in loaves
containing 250 g available carbohydrate. The ingredients for
Table 1 Macronutrient composition of the carbohydrate foods and pistachio test meals in both studies
Test meal
Study 1
White bread (50 g available CHO)
Pistachio 28g
Pistachio 56g
Pistachio 84g
White bread þ 28 g pistachios
White bread þ 56 g pistachios
White bread þ 84 g pistachios
Study 2
White bread (50 g available CHO)
Parboiled rice
Parboiled rice þ 56 g pistachios
Pasta
Pasta þ 56 g pistachios
Instant mashed potatoes
Instant mashed potatoes þ 56 g pistachios
Amount
(g)
Energy
(kcal)
Protein
(g)
Fat
(g)
Total
CHO (g)
Dietary
fiber (g)
Available
CHO (g)
104
28
56
84
104 þ
28
104 þ
56
104 þ
84
245
165
330
495
410
8
6
12
18
14
2
13
26
39
15
53
9
18
27
62
3
3
6
9
6
50
6
12
18
56
575
20
28
71
9
62
740
26
41
80
12
68
245
217
547
8
4
16
2
0
26
53
50
68
3
0
6
50
50
62
246
576
9
21
1
27
53
71
3
9
50
62
221
551
4
16
1
27
50
68
0
6
50
62
104
63
63 þ
56
73
73 þ
56
59
59 þ
56
Abbreviations: CHO, carbohydrate; total CHO: dietary fiber and available CHO.
European Journal of Clinical Nutrition
Pistachios improve post-prandial glycemia
CWC Kendall et al
Data analysis
Incremental areas under the plasma glucose curves were
calculated using the trapezoid rule, ignoring area beneath
the baseline value. The GI or RGR was calculated by
expressing each subject’s glucose incremental areas under
the plasma glucose curves for the test food as a percentage of
the same subject’s average response after consuming the
reference white bread. The mean of the resulting values was
the RGR. To calculate the RGR, based on the glucose scale
(that is, GI of glucose ¼ 100), the RGR bread scale values
were multiplied by 0.71. The blood glucose concentrations at
each time point and the incremental areas under the
plasma glucose curve values were subjected to repeatedmeasures analysis of variance, examining for the effect of
test meal. After demonstration of significant heterogeneity,
the significance of the differences between individual
means was assessed using Tukey’s test to adjust for multiple
comparisons. In addition, the significance of the differences
between blood glucose concentrations and increments for
each test food and white bread were assessed by paired t-test.
To estimate the RGR lowering potential of 1 g of pistachios,
the change in RGR for each study meal was averaged and
calculated per gram of pistachio consumed.
Results
Relative glycemic response
Mean fasting blood glucose was identical before each test
meal within each series. The glycemic response to all three
doses of pistachios was significantly lower at 30, 45, 60 and
90 min after ingestion in comparison with the white bread
control (Po0.01) (Figure 1a). Furthermore, 28, 56 and 84 g of
pistachios had significantly lower RGR in comparison with
white bread (5.7±1.8, 3.8±1.8 and 9.3±3.2 versus 100,
8.0
28 g
56 g
84 g
WB
7.0
6.0
5.0
*
*
*
*
60
90
4.0
3.0
0
Incremental Blood Glucose
(mmol/L)
Blood glucose analysis
Blood samples were stored at 20 1C until analysis, which
took place within 4 days of collection. Blood glucose was
analyzed using a Yellow Springs Instrument Model 2300
STAT (Yellow Springs, OH, USA).
Blood Glucose (mmol/L)
3
each loaf (250 ml warm water, 340 g all-purpose flour, 7 g
sugar, 4 g salt and 6.5 g dry yeast) were placed into the bread
maker according to instructions, and the machine was
turned on. After the loaf was prepared, it was allowed to
cool for an hour, and then weighed and after discarding the
crust ends, the remainder was divided into portion sizes
containing 50 g available carbohydrate. These portions were
frozen before use, and reheated in a microwave before
consumption. Study meals were given in random order.
Palatability was rated on a 100 mm visual analog scale
anchored with ‘very unpalatable’ at one end and ‘very
palatable’ at the other. The higher the number, the higher
was the perceived palatability of the product.
30
4.0
28gP+WB
56gP+WB
84gP+WB
WB
3.0
*
*
2.0
*
1.0
*
*
*
*
0.0
0
30
120
60
Time (min)
*
*
90
120
Figure 1 (a) Glycemic response to white bread (WB; 50 g of
available carbohydrate) and increasing doses of pistachios (28, 56,
84 g) consumed alone. *Significantly different from white bread
(Po0.01). (b) Incremental glycemic response to white bread alone
(WB; 50 g of available carbohydrate) or white bread consumed with
28, 56 and 84 g of pistachios. *Significantly different from white
bread (Po0.01).
respectively; Po0.001) (Table 2). Similarly, adding increasing
doses of pistachios to white bread significantly reduced the
glycemic response at 30, 45, 60 and 90 min for the 84 g dose
(Po0.01), at 45, 60 and 90 min for the 56 g dose (Po0.01)
and at 45 and 60 min for the 28 g dose (Po0.01) in
comparison with the white bread control (Figure 1b). When
pistachio nuts were added to the white bread meal, only the
higher doses, 56 and 84 g, resulted in significant reductions
in the RGR in comparison with the white bread control
(67.3±9.8 (P ¼ 0.009) and 51.5±7.5 (Po0.001) versus 100,
respectively) (Table 2).
In study 2, the addition of 56 g of pistachios to other
commonly consumed carbohydrate rich foods (parboiled
rice, pasta and potatoes) resulted in reduced glycemic
responses (Table 3). When the pistachio meals were compared with their respective control meals, the addition of
56 g of pistachios significantly lowered the RGR of both
parboiled rice (72.5±6.0 versus 58.7±5.1; P ¼ 0.031) and
pasta (94.8±11.4 versus 56.4±5.0; P ¼ 0.025), whereas
the reduction approached significance for instant mashed
potatoes (109.0±6.6 versus 87.4±8.0; P ¼ 0.063) (Table 3;
Figure 2). The mean reduction in glycemic response observed
per gram of pistachios consumed was found to be 0.35 U,
that is, 1 g of pistachios added to a food lowered the RGR of
European Journal of Clinical Nutrition
Pistachios improve post-prandial glycemia
CWC Kendall et al
4
Table 2 Study 1: Palatability and relative glycemic response (RGR) of white bread and pistachio meals (N ¼ 10)
Code
Palatability (mm)
RGR (bread scale)
(RGR)a (glucose scale)
WB
28P
56P
84P
WB þ 28P
WB þ 56P
WB þ 84P
81.8±3.8
83.5±4.7
81.7±5.8
81.1±5.7
79.8±4.3
77.9±5.8
75.2±5.9
100a
5.7±1.8b
3.8±1.8b
9.3±3.2b
89.1±6.0a
67.3±9.8c
51.5±7.5c
71a
—
—
—
63.2±4.2a
47.8±6.9b
36.6±5.3b
Test meal
White bread (50 g CHO)
Pistachio 28g
Pistachio 56g
Pistachio 84g
White bread þ 28 g pistachios
White bread þ 56 g pistachios
White bread þ 84 g pistachios
Values within a column not sharing a common alphabet are significantly different (Po0.01).
a
RGR is presented in both the bread and s glucose scale; to convert the bread scale to the glucose scale multiply by 0.71 (Atkinson et al., 2008).
Table 3 Study 2: comparison of carbohydrate-containing foods consumed alone or with pistachios: palatability, iAUC and relative glycemic response
(N ¼ 10)
Test Meal (Amounts)
White bread (g)
Rice
Rice þ 56 g pistachios
Pasta
Pasta þ 56 g pistachios
Instant mashed potatoes
Instant mashed potatoes þ 56 g pistachios
Code
Palatability (mm)
iAUC
RGRa (bread scale)
WB
Rice
56P þ rice
Pasta
56P þ pasta
Potato
56P þ potato
81.8±3.8a
79.9±5.1a
80.3±5.4a
76.7±4.6a
77.9±5.8a
49.8±5.8b
56.5±7.3b
188.1±22.4a
133.8±17.6b
109.9±15.7b
169.7±21.1a
112.2±22.0b
203.8±27.5a
161.6±23.1a
100a
72.5±6.0a
58.7±5.1b
94.8±11.4a
56.4±5.0b
109.0±6.6a
87.4±8.0a
Abbreviations: iAUC, incremental area under the glucose curve; RGR, relative glycemic response.
Values not sharing a common alphabet are significantly different (Po0.05).
a
RGR is calculated based on bread scale; to convert to the glucose scale multiply by 0.71 (Atkinson et al., 2008).
for foods varying in composition and physical form (for
example, beverages).
120
Palatability
All test meals were well tolerated. Palatability scores of
instant mashed potatoes with or without pistachios were
significantly lower when compared with all the other test
meals (Tables 2 and 3).
100
*
80
*
60
*
40
Discussion
Potato + P
Potato
Pasta + P
Pasta
Rice + P
Rice
0
White Bread + P
20
White Bread
Relative Glycemic Response
140
Figure 2 Relative glycemic response to meals of white bread,
rice, pasta or instant mashed potatoes containing 50 g of available
carbohydrate consumed alone or with 56 g of pistachios. *The
pistachio meal is significantly different from the respective nonpistachio control meal (Po0.01).
that food by 0.35 units on the glucose scale or 0.49 U on the
bread scale. It must be pointed out that these results may
only apply to the foods tested and results may be different
European Journal of Clinical Nutrition
The present study is the first to assess the effect of pistachio
nuts on post-prandial glycemia. The findings confirm the
very low glycemic responses to pistachios eaten alone would
be predicted on the basis of their low available carbohydrate
content (6 g per ounce) and on the results of other nuts
(almonds) and oil seeds (peanuts), (Johnston and Buller,
2005; Jenkins et al., 2006; Josse et al., 2007). Moreover, these
data demonstrate that the addition of pistachios to foods
with high available carbohydrate content reduces the overall
glycemic impact of the foods studied (parboiled rice, pasta,
white bread and mashed potatoes), despite increasing the
overall available carbohydrate content. Of particular interest
was the progressive reduction in bread glycemic response
with the increasing doses of pistachios. The graded glycemic
response reduction of white bread has also been observed
with almonds in a similar dose-response study conducted in
Pistachios improve post-prandial glycemia
CWC Kendall et al
5
healthy individuals (Josse et al., 2007). Pistachios and other
nuts are energy-dense foods, and it has been recognized that
gastric emptying is reduced by a high fat and energy load
such that the pylorus tends to regulate the flow of energy
into the duodenum (Hunt and Stubbs, 1975; Peracchi et al.,
2000). A study by Henry et al. (2008) found that the glycemic
response of bread can be lowered by the addition of any
type of fat. Thus, increasing energy and fat load with an
increasing dose of pistachios would therefore tend to reduce
the glycemic response in a dose-dependent manner as
observed. It is also possible that the addition of pistachios
resulted in a reduction in carbohydrate absorption or altered
the osmotic load and volume of the stomach, all of which
would alter the post-prandial glycemic response. The acute
benefits of pistachios on glycemia observed in the current
study may be indicative of long-term improvements in
glycemic control in light of recent evidence showing that
the addition of 60–100 g of pistachios to a Mediterranean
diet for 4 weeks significantly reduced fasting glucose levels
in healthy adults in comparison with an unmodified
Mediterranean diet (Sari et al., 2010).
The low post-meal glycemic response to pistachios is also
of particular interest in relation to recent studies, indicating
that nut consumption was protective for CVD (Fraser et al.,
1992; Hu et al., 1998; Ellsworth et al., 2001; Kris-Etherton
et al., 2001; Albert et al., 2002). In each of these large
prospective studies, the Physicians’ Health Study (Albert
et al., 2002), the Iowa Women’s Health Study (Ellsworth
et al., 2001), the Nurses’ Health Study (Hu et al., 1998) and
the Adventist Health Study (Fraser et al., 1992), those who
consumed the greatest amount of nuts versus those who
consumed the least had significant reductions in the risk of
death from CVD, relative risk ¼ 0.53, 0.81, 0.65 and 0.52,
respectively. Clinically, post-meal hyperglycemia has been
linked to endothelial dysfunction (Williams et al., 1998;
Kawano et al., 1999) and oxidative stress (Ceriello et al.,
2004); both of which are CVD risk factors. Post-prandial
lipemia has also been associated with an increased risk for
coronary heart disease (CHD). Although consumption of
nuts would increase post-prandial lipemia, a study by Berry
et al. (2008) found that eating whole almonds resulted in a
lower post-prandial rise in plasma triglycerides compared
with almond oil or sunflower oil meals (74 and 58%,
respectively) that were balanced for macronutrients and
fiber. In addition, nuts have a healthy fatty acid profile that
is largely unsaturated and may provide other CHD benefits
beyond reducing the post-prandial glycemic impact of a
meal. Monounsaturated fat tends to raise high-density
lipoprotein cholesterol when exchanged for carbohydrate,
and the Mensink and Katan equation also attribute a small
but important low-density lipoprotein cholesterol lowering
effect to monounsaturated fat (Mensink and Katan, 1992).
This lowering of low-density lipoprotein cholesterol is
supported by a number of studies, which have shown that
pistachios (Edwards et al., 1999; Kocyigit et al., 2006;
Sheridan et al., 2007; Gebauer et al., 2008; Kay et al., 2010;
Sari et al., 2010), almonds (Griel and Kris-Etherton, 2006)
and walnuts (Banel and Hu, 2009) can potentially reduce the
risk of CVD by improving serum lipid concentrations.
The low glycemic effect of nuts may provide a reason for
the inclusion of nuts in diets aimed at reducing the risk of
diabetes as the substitution of nuts for high GI carbohydrates
would reduce the glycemic load of the diet. Furthermore, it
may be beneficial to advise people with Type 2 diabetes to
consume nuts when they consume carbohydrates as part of
their daily diet to reduce the acute, post-prandial glycemic
impact of the meal. These recommendations are supported
by recent recommendations by both the American Diabetes
Association and the International Diabetes Federation,
which emphasize management of post-meal hyperglycemia
as an important component in the management and prevention of Type 2 diabetes (American Diabetes Association
(ADA), 2007; International Diabetes Federation, 2007).
Few studies have assessed the effect of nuts on diabetes risk
and control. Of the two cohort studies, only the results from
the Nurses Health Study cohort (Jiang et al., 2002) but not
the Iowa Women’s Health Study (Parker et al., 2003) indicate
that consumption of five or more servings per week of
nuts compared with rarely or no intake reduces the risk of
developing diabetes (relative risk ¼ 0.73, 95% confidence
interval, 0.60–0.89). Data from clinical studies indicate that
nuts are beneficial in reducing CHD lipid risk factors in
patients with diabetes or the metabolic syndrome (Lovejoy
et al., 2002; Tapsell et al., 2004; Estruch et al., 2006; Li et al.,
2009). In addition, some studies have found a significant
reduction in fasting insulin (Casas-Agustench et al., 2011;
Tapsell et al. 2009) or a significant improvement in insulin
resistance (Casas-Agustench et al., 2011). However, none
have reported a significant reduction in glycated proteins as
a marker of long-term glycemic control (Lovejoy et al., 2002;
Scott et al., 2003; Tapsell et al., 2004; Estruch et al., 2006;
Mukuddem-Petersen et al., 2007; Casas-Agustench et al.,
2011; Tapsell et al., 2009; Ma et al., 2010). In light of recent
evidence showing that the combination of the 2 h post-meal
glucose levels and fasting blood glucose allow for better
estimation of risk both for diabetes and CVD than the fasting
blood glucose alone (Sorkin et al., 2005; International
Diabetes Federation, 2007); further studies that examine
the effect of nuts on post-meal glycemia are warranted.
We conclude that pistachios resulted in a minimal rise in
blood glucose when fed alone over a wide range of
acceptable intake levels. Moreover, they also depress the
blood glucose response to bread in a dose-dependent manner
and the glycemic response of other carbohydrate rich meals,
possibly related to their high fat, fiber and protein content.
In view of their favorable fatty acid profile, their beneficial
effects on serum lipid levels and their low glycemic impact, it
seems now appropriate to assess their effects in longer-term
studies of diabetes. These studies should aim at reducing the
dietary glycemic load to assess whether nut consumption
results in reduced concentrations of long-term biomarkers of
glycemic control, such as glycated proteins. However, it is
European Journal of Clinical Nutrition
Pistachios improve post-prandial glycemia
CWC Kendall et al
6
important to note that in the context of a healthy diet, care
must be taken not to increase calories above requirement
and nuts should be substituted for other foods and not
simply added to one’s diet.
Conflict of interest
David Jenkins has served on the Scientific Advisory Board
of Loblaw Brands Ltd, Sanitarium, Herbalife International,
Nutritional Fundamentals for Health, Pacific Health
Laboratories, Metagenics/MetaProteomics, Bayer Consumer
Care, Almond Board of California, California Strawberry
Commission, Orafti, Unilever and Solae. Cyril Kendall has
served on the Scientific Advisory Board of Paramount Farms.
David Jenkins and Cyril Kendall have received grants from
Barilla, Solae, Unilever, Hain Celestial, Loblaw Brands,
Sanitarium, Almond Board of California, International
Tree Nut Council, California Strawberry Commission, the
Western Pistachio Association, Orafti, and the Canola and
Flax Councils of Canada. David Jenkins has been on the
speakers’ panel for the Almond Board of California. Cyril
Kendall has been on the speakers’ panel for the Almond
Board of California, Paramount Farms and the International
Tree Nut Council.
Acknowledgements
We are grateful to the Western Pistachio Association, Fresno,
CA, USA for provision of the pistachios and for funding
for additional statistics. This work was supported by the
Western Pistachio Association, Fresno, CA, USA and the
California Pistachio Commission. DJAJ is funded by the
Federal Government of Canada as a Canada Research Chair
in Nutrition and Metabolism.
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