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*
Unilever Research Vlaardingen, Vlaardingen, The Netherlands; and
Division of Human Nutrition and Epidemiology, Wageningen Agricultural University, Wageningen, The Netherlands
1To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • carotenoids • lycopene • bioavailability • tomatoes • humans
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Interestingly, the association was strongest for tomato
paste, which was the tomato product that showed the best correlation
with serum lycopene levels. Differences in lycopene bioavailability
among different tomato products may explain this latter observation.
This is supported by the finding that the lycopene response in plasma
or triglyceride-rich lipoproteins
(TRL)2
is higher after consumption of tomato paste than after consumption of
fresh tomatoes (Gärtner et al. 1997
,
Porrini et al. 1998
). The production of tomato paste
from fresh tomatoes involves homogenization and heat treatment.
Previous studies have shown that a combination of these treatments
enhances the bioavailability of carotenoids from vegetables
(Rock et al. 1998
, Van Zeben and Hendriks 1948
). However, up until now, the contribution of each of these
processes has not been clear. As heat treatment can have a deleterious
effect on the micronutrient content of vegetables, it is important to
determine systematically the separate effect of homogenization and heat
treatment on the bioavailability of lycopene and ß-carotene from
tomatoes and the interaction between these two processes.
Various approaches have been used to investigate carotenoid
bioavailability. Most studies have used carotenoid responses in plasma
following 3 to 6 wk supplementation as a measure of carotenoid
bioavailability (e.g., Micozzi et al. 1992
, Rock et al. 1998
,
Törrönen et al. 1996
, Van Zeben and Hendriks 1948
).
Recently, the carotenoid response in the TRL-fraction of plasma was
suggested as a valuable model, because TRL contain newly absorbed
carotenoids (Van Vliet 1996
). A disadvantage of such a
single-dose protocol is the large number of blood samples that need
to be drawn. However, longer term supplementation is also a burden on
the volunteers and labor-intensive. Therefore, we determined whether a
short-term intervention period would be a suitable approach to
estimate carotenoid bioavailability from tomatoes processed in
different ways. We compared the postprandial carotenoid response in the
TRL fraction of plasma after a single consumption with the carotenoid
response in fasting plasma after 4 d consumption of the same
tomato products. The tomato products had been homogenized to different
degrees and heat treated to determine systematically the effect of
these processing conditions on the bioavailability of carotenoids from
canned tomatoes.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Participants were recruited via advertisements in the weekly periodical
of the laboratory, in local newspapers and on local radio and
television stations. Volunteers were employees of Unilever Research
Vlaardingen or inhabitants of the surrounding area. They were eligible
when they met the following criteria: aged between 18 and 70 y;
body mass index (BMI) between 19 and 30 kg/m2; no excessive
use of alcohol (males 
28 glasses/wk, females 21
glasses/wk); intensive sporting activities 10 h/wk; smoking
five cigarettes, cigars or pipes/d. Volunteers were apparently
healthy, as assessed by questionnaire, and they did not use any
medications except oral contraceptives and did not report
gastrointestinal disturbances. Their body weight was stable for at
least the previous 2 mo, and they had not used dietary supplements
(e.g., vitamins or minerals) during the month prior to the start of the
study. Volunteers were excluded if they were adhering to a medically
prescribed, weight loss or vegetarian diet or if they were pregnant or
lactating. Volunteers who were selected for participation in the
postprandial measurement of the carotenoid response in TRL had normal
fasting serum triglyceride concentrations (i.e., <3.0 mmol/L) and
normal whole-blood hemoglobin concentrations (i.e., 
8.0 mmol/L
for males; 7.5 mmol/L for females).
Volunteers received information on the background and design of the study and they gave their informed consent before participation. The protocol of the study was approved by the Medical Ethical Committee of Unilever Nederland BV.
Study design.
The study had a split-plot design with three degrees of
homogenization of the tomatoes (none, i.e., whole tomatoes; mild, i.e.,
blended tomatoes; severe, i.e., tomatoes blended under high pressure)
and two levels of additional heat treatment (minimal, i.e., only
heating before serving; extensive, i.e., 1 h at 100°C before
serving). The effect of homogenization was tested within persons during
three experimental periods and that of additional heat treatment
between persons (Fig. 1
). Thirty-six volunteers were divided in two groups, by gender.
|
A subgroup of 12 participants, 6 for each heat treatment group,
participated in measurements of the postprandial carotenoid response in
the TRL following consumption of the tomato products (Fig. 1)
. On d 1
of each of the three experimental periods, they consumed the
tomato-pasta meals in the morning, instead of at lunch. After a
fasting blood sample had been drawn, they consumed the meal within 30
min. Additional blood samples were taken 2, 3, 4.5, 6 and 8 h
after start of consumption of the experimental meal for measurement of
carotenoids, retinyl palmitate, triglycerides and total antioxidant
activity in the TRL-fraction of plasma. A low-fat,
carotenoid-free lunch was provided after the 4.5-h blood sample.
Based on previous studies, we calculated that the number of volunteers included in the 4-d study would be sufficient to show a 35% difference in plasma lycopene response in the parallel comparison of the heat-treatment effects (CV within subjects 28%; unpublished data). The choice of the number of volunteers for the measurement of the carotenoid response in TRL was based on practical considerations because no data were available on the within-person variation of lycopene responses in TRL.
Tomato products, experimental meals and background diet.
Starting material for the tomato products were peeled and canned whole tomatoes (Lycopersicum esculentum) (Lipton, Stockton, CA). In the factory, these tomatoes had received a 55-min heat treatment at 100°C after canning to ensure microbiological safety. After reaching 100°C in the center of the cans, they had been cooled to about 50°C within 1 h. We did not use fresh tomatoes because the physical and chemical properties of fresh tomatoes may change during storage, and that might have interfered with the effects of processing which we assessed in a cross-over study design over 3 wk.
Mildly homogenized tomatoes were prepared on the experimental days by blending for 2 min (Ultra-Turrax T50; IKA-Labortechnik, Staufen, Germany). Severe homogenization included blending for 2.5 min using the same blender, followed by processing in a high-pressure homogenizer at 200 bar (APV-GAULIN homogenizer, type Lab 60–10 TBS; APV-GAULIN GmbH, Lübeck, Germany). Severely homogenized tomatoes were prepared in one batch before the start of the experiment, and batches of 2.8–3 kg were stored at -20°C until use on the experimental days.
Additional heat treatment was given on the experimental days, just before serving. The minimally additionally heated tomatoes were heated to ~80°C and served immediately thereafter, whereas the extensively additionally heated tomatoes were first boiled for 1 h and then served.
Tomato products were served with macaroni, ham and a white sauce and a
dessert of custard. The total energy content and macronutrient
composition of the meals were the same for all volunteers, and the
total energy content was about 70% of an average Dutch main meal
(Voorlichtingsbureau voor de Voeding 1993
) to ensure that everyone
would be able to consume the complete meal. Participants consumed the
experimental meals under supervision in the kitchen of our laboratory.
They were free to choose their own foods during the rest of each
experimental day. However, they were instructed not to consume products
high in carotenoids, such as vegetables, fruits, fruit juices and
tomato products, or high in vitamin A, such as liver products.
Compliance was assessed by questionnaire.
During the postprandial studies, volunteers consumed no other foods until 8 h after consumption of the experimental meal, except for a standard lunch of low fat and carotenoid and vitamin A-free products 4.5 h after start of consumption of the experimental meal. This lunch was consumed under supervision as well.
Seven days before the start of each experimental period, volunteers received the same instructions with respect to consumption of carotenoid and vitamin A-rich products as during the experimental periods. We supplied them with frozen ready-to-eat meals (Iglo, Veldhoven, the Netherlands), which were low in carotenoids, to replace their hot main meal.
Analysis of tomato products and experimental meals.
Duplicate portions of the complete experimental meals (3 samples per
type), as consumed, were analyzed for macronutrient and fiber content.
The meals were formulated to provide 157 µg of preformed retinol
(Holland et al. 1991
). The carotenoid content of the
tomato products (9 samples per type) was determined by HPLC on a ET
200/4 nucleosil 100–5CN column (Machery & Nagel, Duren, Germany).
After extensive extraction (five times, until the last extract was
colorless) with tetrahydrofurane/methanol (1:1, v/v),
ethyl-ß-apo-8'-carotenoate was added as internal standard.
ß-Carotene and lycopene were separated by gradient elution with
n-heptane/4% isopropanol 0–3 min 97.5:2.5 (v/v); 3–15
min change from 97:2.5 to 50:50 (v/v); 16–30 min 97.5:2.5 (v/v) at a
flow rate of 1.0 mL/min and a column temperature of 20°C. The eluent
was monitored by UV-Vis detection at 450 nm for ß-carotene and at
470 nm for lycopene. In this system, 
-carotene coelutes with
ß-carotene. Because tomatoes contain no -carotene (Khachik et al. 1992
), the HPLC response is considered to be
ß-carotene. Table 1
shows the macronutrient and fiber content of the experimental meals and
the carotenoid content of the tomato products.
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shows photographs of representative samples of the homogenized tomato
products. The majority of the cells were intact in the minimally
additionally heated tomatoes, whereas after severe homogenization,
and/or extensive additional heat treatment, many of the cell walls were
no longer intact. Heat treatment had a less destructive effect than
severe homogenization, as more cells were still intact after extensive
heat treatment only.
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Mild extraction of lycopene was used as an in vitro test to estimate
the in vivo release of this carotenoid from tomatoes. Ca. 1 g of
tomato product was mixed thoroughly by using a vortex during 1 min with
3 mL n-heptane. After 30 min at room temperature in the
dark, the sample was mixed again on a vortex for 1 min and subsequently
centrifuged at 1000 x g for 3 min. The supernatant
was collected, the residue was mixed with n-heptane for
1 min on a vortex and immediately thereafter centrifuged. Lycopene
content of the extracts was determined by spectophotometry (UV 2101 PC;
Shimadzu Corporation, Tokyo, Japan) at 470 nm, using an
extinction coefficient of 3450 L · mol-1 ·
cm-1. The release of lycopene was calculated as the amount
of lycopene measured after mild extraction expressed as proportion of
the amount measured after extensive extraction (Table 1)
.
Collection and analysis of blood samples.
Blood samples were obtained from fasting subjects before and after each
of the 4-d experimental periods. In a subgroup, additional samples were
collected for measurement of the carotenoid response in TRL after
consumption of the experimental meal. Blood samples were collected into
sodium EDTA-coated tubes, and plasma was separated by
centrifugation at 1500 x g for 10 min at room
temperature. Plasma samples were stored at -80°C until analysis or
isolation of the TRL-fraction. Isolation of the TRL-fraction
was performed as described by Van Vliet et al. (1995)
. After thawing,
3.5 mL plasma was overlayered with 8 mL NaCl (9 g/L; d = 1.004
kg/L) The samples were centrifuged for 1 h at 150,000 x g at 20°C in a Beckman L8–60M ultracentrifuge
(Beckman Instruments, Palo Alto, CA). The TRL-containing fraction
was then removed (2.1 mL) and stored at -80°C until further analysis
within 6 wk.
Prior to analysis of the carotenoid and retinyl palmitate content, the TRL-fraction was extracted with n-heptane/ether (3:1, v/v). Carotenoid concentrations in plasma and carotenoid and retinyl palmitate concentrations in TRL were determined by HPLC on a nucleosil 100 5CN column (Machery & Nagel) with n-heptane as mobile phase at a flow rate of 0.7 mL/min. Ethyl-apo-8-carotenoate was used as internal standard. UV-Vis detection was used to monitor concentrations of lycopene at 470 nm, ß-carotene at 450 nm and retinyl palmitate at 325 nm. Intra-assay variation was 4.5% for lycopene and 3.9% for ß-carotene in plasma.
The ferric-reducing ability of plasma (FRAP) and the
TRL-fraction were determined as a measure of total antioxidant
activity, as described by Benzie and Strain (1996)
. Total cholesterol
and triacylglycerol concentrations in plasma and triglyceride
concentrations in the TRL-fraction were assessed by using
commercially available colorimetric test kits (plasma cholesterol:
CHOD-PAP, Boehringer, Mannheim, Germany; plasma triacylglycerol:
GPO-PAP (Roche, Basel, Switzerland)/GPO-Trinder (Sigma, St. Louis,
MO); triglycerides in TRL: Unimate 5 TRIG kit (Roche).
Statistical evaluation.
The data obtained were normally distributed as determined by visual evaluation. The data were analyzed using ANOVA with persons (within heat treatment) and period as blocks and heat treatment (minimal or extensive) and degree of homogenization (none, mild or severe) as factors in a split-plot model. The significance of the treatment effects on the in vitro release of lycopene from the tomato products was determined by two-way ANOVA with heat treatment and degree of homogenization as factors. If a significant interaction was found between the effect of additional heat treatment and degree of homogenization, their effects were tested separately. For the carotenoid responses in the TRL-fraction, the statistical analysis was performed with and without the triglyceride response included as covariable. The responses considered were changes in plasma concentrations and changes from baseline in TRL concentrations at each time point as well as the area under the curve of the concentrations in TRL. Treatment effects on carotenoid responses in plasma and TRL and antioxidant activity in TRL were tested one-sided, based on the hypothesis that a more extensive heat treatment or more severe homogenization would induce larger responses. For all other variables (i.e., plasma lipid concentrations, antioxidant activity of plasma, triglyceride and retinyl palmitate concentrations in TRL and in vitro lycopene release), differences among treatments were tested two-sided. P-values < 0.05 were considered significant.
Results are expressed as means (SD) for descriptive variables and as least square means (SE) for all other variables.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Thirty-three participants completed the study (Table 2
). One subject dropped out before the start of the study for unknown
reasons, and two others did not complete the study due to illness.
Eleven volunteers participated in the measurement of the
TRL-responses. Only two of the 33 volunteers smoked ( 5
cigarettes/d).
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A significant difference was found in lycopene extractability from the
different tomato products which was assessed as the percentage of
lycopene extracted after mild heptane treatment as compared to the
contents measured after extensive extraction (see Table 1
). Both
additional heat treatment and homogenization enhanced the release of
lycopene during mild extraction. However, as 100% release was already
reached by minimally heated, severely homogenized tomatoes, additional
heat treatment did not further enhance the release of lycopene from the
severely homogenized tomato products (Fig. 3
).
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The triglyceride responses in the TRL-fraction of plasma were not
significantly different among the treatments (Tables 3
and
4), and inclusion of the triglyceride response as covariable did not
change the treatment effects on carotenoid responses in TRL. Therefore,
here we consider the treatment effects on the carotenoid responses
without correction for triglyceride concentrations.
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and Fig. 4
). Additional heat treatment also tended to induce a larger
TRL-response of lycopene and ß-carotene (P = 0.14, Table 4
and Fig. 5
). The change in ferric reducing ability of the TRL reflected the
changes in carotenoid concentration (Figs. 3
, 4)
. Homogenization
significantly improved the antioxidant activity of TRL (Table 3)
,
whereas the effect of additional heat treatment was not significant
(Table 4)
. The responses of retinyl palmitate (results not shown) were
not significantly different among the different treatments.
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The effect of homogenization and heat treatment on the change in
fasting plasma lycopene concentrations following 4 d of consuming
the differently processed tomatoes were similar to those found for the
lycopene response in TRL after single consumption. We observed
significantly larger plasma lycopene responses with increasing degree
of homogenization (Table 3)
. Further, additional heat treatment tended
to increase the plasma lycopene response (P = 0.17,
Table 4
).
There was a significant interaction between the effects of the degree
of homogenization and those of additional heat treatment on the plasma
response of ß-carotene. Homogenization enhanced the plasma response
of ß-carotene only if the tomatoes were not given additional heat
treatment (Table 5
). Furthermore, a significant effect of additional heat treatment was
found only for whole tomatoes, whereas it did not enhance the plasma
ß-carotene response induced by homogenized tomatoes.
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and 4)
. Total cholesterol and
triacylglycerol concentrations in plasma were unaffected (results not
shown). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Comparison of carotenoid responses in TRL and plasma.
The use of the postprandial carotenoid response in the TRL-fraction
of plasma as a measure of carotenoid absorption is based on the fact
that carotenoids present in chylomicrons originate directly from the
enterocytes. In contrast, in experiments with repeated carotenoid
consumption, changes in fasting plasma carotenoid concentrations are
not only affected by the amount of carotenoids absorbed, but also by
carotenoid metabolism, tissue distribution and transfer of carotenoids
between lipoproteins in blood. As mentioned above, we found similar
differences in lycopene responses in plasma and TRL among the different
treatments. This indicates that both approaches can be used to
determine the effects of tomato processing on lycopene bioavailability.
However, the sizes of the differences found between TRL responses were
generally larger than those found between plasma responses. In
addition, the number of volunteers required to show significant
treatment effects was larger for the 4 d plasma response. This
indicates that the postprandial lycopene response in TRL is more
sensitive than the response in plasma after 4 d consumption. The
plasma response is thus best applied if large differences are expected
among treatments and/or if a larger number of volunteers can be
included in the study. With respect to ß-carotene, the results were
slightly different because we found a significant interaction between
the degree of homogenization and additional heat treatment for the
response of ß-carotene in plasma but not in TRL. This suggests that,
in contrast to lycopene, for ß-carotene bioavailability, the
postprandial TRL-response is a less sensitive measure than the
plasma response after 4 d. It should be noted however, that the
ß-carotene intake was low (i.e., 1 mg, see Table 1
).
Four days is not sufficient to achieve a new steady state in plasma
carotenoid concentrations, as this takes at least 3 wk (Micozzi et al. 1992
). The differences we observed after 4 d will
relate to those observed after longer intervention although,
quantitatively, they may differ. However, a short intervention period
has several advantages. It is less labor-intensive and compliance
with instructions is probably better during a short period. In contrast
to a single-dose design, it is possible to apply more realistic
conditions and investigate the effect of the test meals as part of a
normal diet. This latter aspect may be particularly relevant.
We found a second peak in carotenoid concentrations in TRL following
the consumption of a second carotenoid-free, low-fat meal after the
4.5-h blood sample. This was also reported by Borel et al. (1998)
, who
used a comparable design. In studies where only one meal was supplied,
only one peak at 4–7 h was found (O’Neill and Thurnham 1998
, Van den Berg and Van Vliet 1998
,
Van Vliet et al. 1995
). Borel et al. (1998)
explained
their finding by the larger ß-carotene content of their test meal as
compared to the earlier studies (i.e., 120 mg vs. ca. 15 mg,
respectively). In the present study, we supplied 21–23 mg lycopene
(Table 1)
. The amount of fat in our test meals was less than that used
by others (i.e., 23 g vs. 43–50 g). Consequently, the
triglyceride content of the TRL was lower. This may have reduced our
initial carotenoid responses due to a limited capacity of chylomicrons
to take up carotenoids, as suggested by Borel et al. (1996)
. Part of
the initially absorbed carotenoids may have remained in the enterocytes
and entered the bloodstream following the uptake of the second meal.
Effects of homogenization and heat treatment.
The extent to which the food matrix, in which carotenoids are
incorporated, is intact is an important determinant of carotenoid
bioavailability as indicated by the present results. The first steps of
carotenoid absorption include disruption of the food matrix,
mechanically and by digestive enzymes, and the subsequent release of
the carotenoids from this matrix and from protein complexes
(Britton 1995
). Homogenization and heat treatment
disrupt cell membranes, whereas heat treatment has been suggested to
disrupt further the protein-carotenoid complexes (Erdman et al. 1988
). Previous studies have shown that homogenization or a
combination of homogenization and heat treatment enhances carotenoid
bioavailability from vegetables in humans (Gärtner et al. 1997
, Porrini et al. 1998
, Rock et al. 1998
, Törrönen et al. 1996
,
Van Zeben and Hendriks 1948
). Our results indicate that
the difference in carotenoid bioavailability from tomato paste vs.
fresh tomatoes (Gärtner et al. 1997
,
Porrini et al. 1998
) can be explained by alterations of
the cellular matrix of tomatoes, probably due to the effect of both
homogenization and heat treatment. It should be noted however, that we
used canned instead of fresh tomatoes as the null condition.
The canned tomatoes used were heated for 55 min at 100°C during
manufacturing. Further processing was still able to enhance the
bioavailability of carotenoids from these tomatoes significantly,
despite the processing steps which had previously been applied. As
anticipated, homogenization under high pressure was more effective in
increasing carotenoid bioavailability than homogenization under normal
pressure. As shown in Figure 2
, in part of the cells, the cell walls
were still intact after mild homogenization, whereas high-pressure
treatment destroyed the majority of the cell structures. The release of
carotenoids from intact cells is thus indeed a limiting factor for
carotenoid uptake. This confirms data from Van Zeben and Hendriks (1948)
, who found that homogenization of cooked carrots enhanced the
bioavailability of ß-carotene as measured by changes in plasma
concentrations.
Published data on the effects of heat treatment on the bioavailability
of carotenoids from vegetables are not consistent. A study in ferrets
found no significant differences in ß-carotene responses following
consumption of unheated or heated carrot juice or carrot chromoplasts
(Zhou et al. 1996
). In another study with preruminant
calves, Poor et al. (1993)
found an enhanced ß-carotene reponse when
steamed homogenized carrots were compared with raw homogenized carrots,
although this effect was not significant. As the cellular matrix of the
carrots had been disrupted most in case of the carrot juice, these
results may indicate that heat treatment is more effective for less
homogenized carrots. That would be in line with our observation of an
enhanced plasma ß-carotene response by additional heating of whole
tomatoes but not homogenized tomatoes. Also, the amount of
cis-isomers of ß-carotene may have interfered with these
findings as heat treatment can induce in
cis-trans isomerization in tomatoes
(Nguyen and Schwartz 1998
). The responsiveness of plasma
concentrations of all-trans ß-carotene to supplementation
is larger than that of cis-isomers (Gaziano et al. 1995
, Tamai et al. 1995
). However, we could not
quantify the presence of cis-isomers of ß-carotene with
the analytical method used.
The increases in carotenoid concentrations in TRL were accompanied by
an increase in the total antioxidant activity of the TRL-fraction
of plasma (Figs. 3C
and 4C
). In contrast, no
significant differences were found in fasting plasma after 4 d.
Uric acid accounts for 60% of the variation in the FRAP (Benzie and Strain 1996
, Cao and Prior 1998
). As TRL do
not contain uric acid or other endogenous antioxidants, the sensitivity
of this fraction of plasma to show differences in antioxidant uptake
may be larger than that of plasma itself. The implication of such a
postprandial increase in ferric-reducing ability for the overall
antioxidant status remains however to be established.
In conclusion, the cellular matrix of tomatoes, which can be disrupted by mechanical homogenization and/or heat treatment, determines the bioavailability of carotenoids. The carotenoid response in plasma after 4 d of consumption can be used to compare the bioavailability of carotenoids from different foods. This conclusion is based on the finding that the treatment effects shown were similar to those found in postprandial changes of carotenoids in TRL.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Manuscript received August 27, 1999. Initial review completed October 14, 1999. Revision accepted December 23, 1999.
|
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