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Institut für Physiologische Chemie I and Biologisch-Medizinisches Forschungszentrum, Heinrich-Heine-Universität Düsseldorf, D-40001 Düsseldorf, Germany;
*
Institut für Experimentelle Dermatologie, Universität Witten-Herdecke, D-58455 Witten, Germany; and
Unilever Health Institute, Unilever Research Vlaardingen, The Netherlands
2To whom correspondence should be addressed. E-mail: wilhelm.stahl{at}uni-duesseldorf.de.
| ABSTRACT |
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16 mg/d of
lycopene, was ingested with 10 g of olive oil over a period of 10
wk by 9 volunteers. Controls (n = 10) received
olive oil only. Erythema was induced by illumination of dorsal skin
(scapular region) with a solar simulator at the beginning of
the study, after 4 wk and after 10 wk. Intensity of erythema was measured
by chromatometry; the a-value was determined directly before and
24 h after irradiation. Serum carotenoid levels were measured by
HPLC. At the beginning of the study, carotenoid levels did not
differ between the two groups. Serum levels of lycopene
increased in supplemented subjects; the other carotenoids did not
change significantly, and no change in serum carotenoids was observed
in the control group. At wk 10, dorsal erythema formation was 40%
lower in the group that consumed tomato paste compared with controls
(P = 0.02; Wilcoxon-Mann-Whitney test). No
significant difference between groups was found at wk 4 of treatment.
The data demonstrate that it is feasible to achieve protection against
UV lightinduced erythema by ingestion of a commonly consumed dietary
source of lycopene.
KEY WORDS: lycopene sunburn skin carotenoids erythema humans
| INTRODUCTION |
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Carotenoids are lipophilic micronutrients with antioxidant activities,
occurring in human blood and tissues, including the skin and the eye
(6
,7)
. Carotenoids in humans originate from intake of
fruits, vegetables and dairy products. There are correlations between a
high intake of a diet rich in carotenoids and the occurrence of several
degenerative diseases (8)
. Such potential protective
effects of carotenoids are thought to be related to their antioxidant
properties (9)
. In vitro studies showed that carotenoids
are among the most effective naturally occurring quenchers of
1O2, with bimolecular rate
constants in the range of
109-1010
(mol/L)-1 · s-1
(10
11
12)
. In addition, carotenoids interact with peroxyl
radicals, thus inhibiting the process of lipid peroxidation
(13
,14)
. Several in vitro studies indicate that among the
natural carotenoids, lycopene is the most efficient antioxidant
(10
,15)
.
ß-Carotene has been used as a so-called oral sun protectant due
to its antioxidant properties, and its efficacy has been shown in human
studies (16
17
18
19)
. After administration of a ß-carotene
supplement for 8 wk, there was a 35% lowering of erythema compared
with pretreatment response toward a 1.5 individual minimal erythema
dose (MED) (19)
. The MED is the minimal amount of energy
required to induce a uniform, clearly demarcated erythema response,
with a maximum
24 h after irradiation.
Tomatoes and tomato products are the major source of lycopene in the
human diet in Western countries (20)
. Bioavailabilty of
lycopene from tomato paste is higher than from other natural sources
such as tomato juice or fresh tomatoes (21)
.
On the basis of the pronounced antioxidant activities of lycopene and its enhanced availability from tomato paste, we investigated whether protection against UV-induced erythema can be provided by dietary intervention with tomato paste.
| SUBJECTS AND METHODS |
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Healthy adults (n = 22), 2667 y old (8 men and 14
women), skin type II, took part in the study. Subjects were recruited
by retrieval of names from a list of volunteers available to the
Institute of Experimental Dermatology (Universität
Witten-Herdecke); they were assigned randomly to the control group or
the group that received tomato paste. Skin-type grading was
according to skin coloration, hair and eye color, and history of
sensitivity toward sun exposure (22)
. Skin type II
criteria were white skin, blonde or light-brown hair, blue eyes,
sensitivity to sun exposure and minimal tanning.
Subjects smoking >3 cigarettes/d were not included in the study; moderate alcohol consumption was allowed. Further exclusion criteria were as follows: history of malabsorption diseases, liver diseases, diseases of lipid metabolism or photosensitivity disorders. No medication was allowed during the study. Written informed consent was obtained from each participant. The study design was approved by the ethics committee of the University of Witten-Herdecke.
The control group received 10 g olive oil/d, which was taken with
the main meal. The tomato paste group ingested 40 g tomato paste/d
with 10 g olive oil, providing
16 mg lycopene, 0.5 mg
ß-carotene and 0.1 mg lutein. The diet was not standardized, but the
participants were advised not to change their dietary habits during the
study. No further supplementation with vitamins or carotenoids was
allowed. Compliance was checked by questionnaire (two times during the
study) and by analyses of serum carotenoid concentrations. The skin
sensitivity of one subject changed substantially during the study,
probably due to increased melanin production as a consequence of skin
tanning by UV exposure. This individual did not develop an erythema and
was excluded. Two subjects did not complete the study for personal
reasons not related to the treatment.
Blood collection and analyses.
Blood samples were collected on d 0 and after 4 and 10 wk of treatment.
Serum was prepared from the blood samples and stored at -20°C until
analysis. The analyses of carotenoids in serum were performed by HPLC
as described (23)
. The content of carotenoids in the
tomato paste was determined as described earlier (21)
.
Skin carotenoid levels were determined by means of reflection
spectroscopy (24)
. The palm of the hand was chosen for
skin measurements.
Induction of erythema and measurement of skin color.
Irradiation with UV light to induce erythema was applied only to dorsal
skin (scapular region) using a solar simulator (SOL3 Hönle,
Munich, Germany). Individual MED was determined for each subject before
the study. On d 0 and after wk 4 and wk 10, the skin of the
participants was irradiated with 1.25 MED. Skin color was evaluated by
chromatometry (Chromatometer Minolta CR 200, Ahrensburg, Germany) using
the three-dimensional color system (L-, a-, b-values). The
L-value is a parameter for lightness of skin, the b-value
(blue/yellow axis) is indicative of pigmentation. The a-value
(red/green-axis) is a measure of erythema formation and the
a-value
(a-value 24 h after irradiation minus a-value before
irradiation) was used to quantify skin responses toward UV-irradiation.
Statistics.
Statistical analysis was performed with the program Biostatistik (Glantz, version 4.02; Maidenhead, UK). The Wilcoxon-Mann-Whitney test was used for comparison of control and treatment groups. The Wilcoxon test was applied to check trend compared with pretreatment in each group. Differences were analyzed at each time point and were considered significant when P < 0.05. Data are presented as means ± SEM.
| RESULTS |
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Increases in serum lycopene levels were observed upon daily ingestion
of 40 g tomato paste, providing about 16 mg lycopene/d
(Table 1
). No change in serum lycopene level was observed in the control group;
individual changes in serum lycopene levels were within 20% of the
initial value. The control and tomato paste groups differed at wk 4
(P = 0.002) and wk 10 (P = 0.002). All
other carotenoids analyzed, including ß-carotene,
-carotene,
lutein, zeaxanthin and cryptoxanthin, did not differ between groups or
change within a group over time. Skin levels of total carotenoids
decreased in the control group (Table 1)
.
|
The
a-values did not differ between the groups at the start or at wk
4 of the experiment (Table 1)
. However, at wk 10, the
a-values of
the treatment group (3.8 ± 1.1) were significantly lower
(P = 0.02) than those of the controls (6.3 ± 0.7), indicating a 40% protection against UV-induced erythema
formation upon ingestion of tomato paste. In the treatment group, the
a-value at wk 10 was significantly lower than at wk 0.
| DISCUSSION |
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Baseline serum levels of lycopene were similar in the two groups and
were within the range reported in the literature (25)
.
Lycopene levels increased in the serum of subjects by 0.35
µmol/L after 10 wk of tomato paste consumption, rising
from 0.37 to 0.72 µmol/L; no significant change occurred
in the control group. The increase found in the present study is
comparable to data from the literature (26
27
28)
, i.e.,
after intake of tomato puree providing 16.5 mg lycopene/d for 3 wk, an
increase of plasma lycopene levels by 0.5 µmol/L (from
0.3 to 0.8 µmol/L) was reported (26)
. The
consumption of tomato juice, providing 40 mg lycopene/d for 2 wk,
resulted in plasma levels of
0.7 µmol/L
(27)
. From the literature it appears that serum or plasma
lycopene concentrations do not exceed 1 µmol/L after
dietary lycopene intake (27
,28)
. Little information is
available on the bioavailability of lycopene from different sources.
After ingestion of
70 mg lycopene/d for 4 wk from tomato juice,
oleoresin or beadlets, similar increases in plasma lycopene levels of
0.24 µmol/L were reported (29)
.
Significant increases in serum and skin levels were observed after the
use of ß-carotene supplements (24)
. Treatment with doses
of
25 mg ß-carotene/d for 12 wk led to serum ß-carotene levels
of 1.8 µmol/L and skin levels of
1.0
µmol/g on the palm of the hand.
The lack of increase in skin lycopene levels (palm of the hands) in
subjects consuming tomato paste might be due to the low bioavailability
of lycopene from this dietary source. Additionally, variations in the
reflection photometry measurements might contribute to and possibly
explain the significant decrease of total skin carotenoids in the
control group. The latter might also be related to seasonal variations
in dietary carotenoid levels. It should be noted that the
a-values
in all groups and at all time points were negatively correlated with
the lycopene levels in serum (0.025 < P < 0.05).
No significant correlation was found between
a-values and skin
carotenoids (0.05 < P < 0.1).
Erythema formation as an indicator of the sunburn reaction was 40%
lower in subjects who ingested tomato paste for 10 wk compared with the
controls. Compared with the initial value within the group, the
a-value was diminished by 32% at wk 10 of supplementation.
The protective effect observed in the present study for
lycopene-rich tomato paste is consistent with data from other
studies that reported protection against erythema formation upon
supplementation with ß-carotene (17
18
19)
. Compared with
the pretreatment response upon irradiation with 1.5 MED, erythema
formation on dorsal skin was diminished by
35% after daily
ingestion of a supplement containing 24 mg ß-carotene for 8 wk
(19)
. No protection was observed in another study using 90
mg/d ß-carotene supplements for 3 wk (30)
. This might be
due to the short treatment time in the latter study. Consistent with
other studies, we found little if any protection after 4 wk of
intervention.
This is the first study demonstrating that intervention with a normal dietary constituent rich in lycopene protects skin against UV-induced erythema formation. Although the efficacy of protection is not comparable to the use of a sunscreen with a high sun protection factor, dietary intake may provide basal protection. Much of the UV exposure over a life time occurs when the skin is not protected; thus, the use of dietary factors with sun-protecting properties might have a substantial beneficial effect.
| FOOTNOTES |
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Manuscript received November 20, 2000. Revision accepted February 27, 2001.
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