Carotenoids in Human Skin: Comparison
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Please note this is a comparison between Version 2 by Beatrix Zheng and Version 1 by Maxim Darvin.

Carotenoids having ≥10 π-π-conjugated C=C double bonds serve as an objective marker of the antioxidant status of human stratum corneum (SC) in vivo according to the principle: the higher the concentration of carotenoids the higher the antioxidant status of the entire SC. The exposure to doses of radiation in the visible (>50 J/cm2) and near-infrared (>120 J/cm2) spectral ranges cause the formation of free radicals in human skin, which can be determined in vivo by a decrease in the concentration of carotenoids in the SC. The topical application of sunscreen containing antioxidants has a protective effect on the skin. A diet containing antioxidants, in particular fruit and vegetables or food supplements, leads to an increase in the carotenoid concentration and the antioxidant status of the SC. The concentration of carotenoids in the SC can reflect the individual lifestyle habits and health status. Resonance Raman spectroscopy and diffuse reflectance spectroscopy are optical methods that provide a rapid and non-invasive screening of the kinetics of carotenoids and changes in the antioxidant status of the human SC, which can be useful in in vivo skin research.

  • beta-carotene
  • lycopene
  • zeaxanthin
  • stratum corneum
  • antioxidant status
  • free radicals
  • reactive oxygen species
  • lipid oxygen species
  • aging
  • nutrition

1. Antioxidants in the Human Skin

The human body in general and the skin in particular contain a balanced set of antioxidants, which can be divided into two main classes—endogenous and exogenous antioxidants [[1],[2]]. The major enzymatic endogenous antioxidants include glutathione peroxidase, catalase, and superoxide dismutase [[3],[4],[5]]. Non-enzymatic endogenous antioxidants include glutathione, lipoic acid, uric acid, coenzyme Q10, vitamin D, intracellular reducing agents nicotinamide adenine dinucleotide (NAD), and nicotinamide adenine dinucleotide phosphate (NADP). Exogenous antioxidants enter the human organism only by nutrition (dietary antioxidants), such as carotenoids; vitamins A1, A2, C, and E; polyphenols; zinc; and selenium [[1],[6],[7],[8],[9],[10],[11],[12]]. Additionally, antioxidants can be divided into water-soluble and fat-soluble antioxidants (Figure 1).

/media/item_content/202208/62f06cfe191b1antioxidants-11-01451-g001.png
Figure 1.
Classification of antioxidants in the skin. “
ws
”—water-soluble, “
fs”—fat-soluble antioxidants [
”—fat-soluble antioxidants
[13]].
.

Most antioxidants are able to neutralize several free radical attacks before being destroyed [[14],[15],[16]]. Some combinations of antioxidants, such as carotenoids and vitamin E [[17]], carotenoids and polyphenols [[18]], superoxide dismutase and catalase [[1],[3]], lycopene, β-carotene, and vitamins C and E [[19],[20]], act in synergy, significantly increasing the number of neutralized free radicals and thus improving the efficiency of antioxidant protection.

Human skin contains a balanced set of antioxidants. Their concentration may vary with the seasons [[21],[22]] and depends on lifestyle habits [[5],[22]]. All of the known methods for determining the concentration of enzymes in the skin are invasive or minimally invasive [[7],[21]]. The mechanisms of SC saturation with enzymatic antioxidants are not well understood; however, superoxide dismutase and catalase are known to be non-homogeneously distributed throughout the human SC, having a minimum near the surface [[4],[21]]. Non-enzymatic endogenous intracellular reducing agents are mainly present in the viable epidermis and in the dermis in various concentrations. The SC contains significantly lower concentrations of enzymatic and non-enzymatic endogenous antioxidants. Thus, non-enzymatic exogenous antioxidants predominate in the SC, continuously entering the cells of the viable epidermis from the bloodstream and saturating the entire SC in the course of keratinization. However, this pathway is not unique, as vitamin E [[23],[24]], the vitamins A1 and A2 [[9]], and carotenoids [[25],[26]] reach the skin surface as part of the sweat and/or sebum secretion and thus increase antioxidant concentrations in the superficial SC [[25],[27],[28]].

2. Carotenoids in Human Skin

Carotenoids are fat-soluble compounds, which are categorized into two classes—xanthophylls containing oxygen and carotenes, which do not contain oxygen [[29]]. Most carotenoids contain 40 carbon atoms and are capable of neutralizing reactive oxygen species (ROS) due to their antioxidant properties as shown in vitro [[30],[31],[32],[33],[34],[35],[36],[37]]. Among carotenoids, lycopene has the highest antioxidant efficiency [[38],[39]], followed by α-carotene, β-cryptoxanthin, β-carotene, zeaxanthin, and lutein [[40]]. Furthermore, carotenoids are natural filters of high-energy visible light, because due to the presence of more than 10 π-π-conjugated C=C double bonds [[41]] they effectively absorb light in the violet-green spectral range [[32],[42]].

In the human body, apart from the skin, carotenoids are found in the blood plasma and are constantly circulating in the bloodstream [[43],[44]]; they are also stored in the subcutaneous fatty tissue [[9],[45]] and the liver [[46]]. The skin carotenoids α-carotene, β-carotene, and γ-carotene are pro-vitamin-active [[47],[48]].

In the human skin, the highest concentration of carotenoids is found within adipocytes in the fat-rich subcutaneous tissue [[49],[50]] and in the SC within the lipid lamellae [[25],[51]]. The carotenoid concentration is non-homogeneously distributed in the SC and has two maxima—near the surface and near the bottom of the SC [[25],[52]], which is explained by the two independent delivery pathways: from the inside due to keratinization and from the outside with sweat and/or sebum secretion [[26],[27],[28],[53]].

3. Methods of Non-Invasive In Vivo Determination of Carotenoids in the SC

Carotenoids can be determined by analyzing skin biopsies using high-pressure liquid chromatography [[45],[54]], but this method is invasive and does not provide accurate information due to preparation-induced oxidation of carotenoids. Non-invasive methods to assess the carotenoid content in the SC in vivo are advantageous and currently popular in skin research due to their practicability and reliability. The most effective non-invasive methods to measure carotenoids in the human SC are limited to optical methods, which include resonance Raman spectroscopy (RRS) [[54],[55],[56],[57]], confocal Raman micro-spectroscopy [[25],[27],[52],[58],[59]], skin color measurements [[60],[61],[62],[63],[64],[65]], and diffuse reflectance spectroscopy [[66],[67],[68]], reviewed in detail in [[69]].

As the concentration of carotenoids in the SC is the highest compared to viable epidermis and dermis [[9]], it is advantageous to measure on the palms of hands, which provide a thick SC and are easily accessible. Skin on other body areas is also suitable for in vivo measurements using exemplary methods.

4. Carotenoids Are Marker Substances of the Antioxidant Status of the Human SC In Vivo

The human SC contains various antioxidants forming the antioxidant status of the SC (Figure 1). Determining the antioxidant status of the SC in vivo requires determining the efficiency of neutralizing free radicals. Electron paramagnetic resonance (EPR) spectroscopy is a non-invasive method for the detection of radical formation in tissues, organs, and cell cultures. The topical application of the spin probe nitroxide TEMPO (2,2,6,6-tetramethylpiperidine-1-yl-oxyl) on the skin allows statements about the redox state in the SC as shown for in vivo measurements on the skin of the human inner forearm [[70]]. The intensity of the EPR signal is proportional to the concentration of the spin probe TEMPO in the SC and decreases exponentially with time. A decrease in the spin probe concentration, according to Hee et al. [[71],[72]], can be described by the radical marker quenching rate constant k, which directly depends on the antioxidant status of the SC.

Thus, the higher the antioxidant status of the SC, the faster the neutralization of TEMPO and the faster the EPR signal intensity decreases and, consequently, the higher is the rate constant k. A positive correlation (R = 0.65) between the concentration of carotenoids and the decrease of the skin probe TEMPO is given implying that the more carotenoids are in the SC, the higher the rate constant k, i.e., the higher is the antioxidant status of the SC. These dependencies confirm that carotenoids can be considered as marker substances of the entire antioxidant status of the human SC of non-smokers in vivo [[73]], which was indirectly confirmed in other studies [[74],[75],[76]]. The obtained results are important for an easier investigation of the changes in the entire antioxidant status of the human SC in vivo based on the determination of the carotenoid concentration, which substantially extends the number of practical applications.

5. Factors Resulting in the Reduction of Carotenoids in the SC

External and internal stress-factors on human skin can result in the formation of free radicals which cause the decrease of antioxidant concentrations in all skin layers [[74]].

One of the main external stress factors is solar radiation. The effect of sunlight on the skin depends on the energy of the photons, the radiation dose and the penetration depth, which is minimal for UV and maximal for the IR-A spectral range. Air pollution by various gases and particulate matter has a negative effect on human skin [[77]] and can also act as an external stressor, leading to the formation of free radicals in human skin [[78]]. To protect the skin from the negative effects of external pollutants, topical application of antioxidants is effective [[79]]. Internal stressors include lifestyle habits such as smoking, alcohol abuse, high-intensity exercise, stress, and dietary habits, as well as diseases.

5.1. Effect of UV Radiation

Under the irradiation with UV-B (dose 0.03 J/cm2: light intensity 0.3 mW/cm2, irradiation time 100 s), a decrease of the carotenoid concentration in the human SC over time was demonstrated in vivo using RRS [[80]]. A decrease of the lycopene / ß-carotene concentration is observed 0–30 / 30–90 min after termination of irradiation, which is probably caused by different quenching rates in the neutralization of ROS. The maximal decrease was observed 2–3 h post-irradiation, which seems to be related to the induction of inflammatory reactions and the subsequent oxidative stress. The recovery of carotenoids in the SC to the initial level lasted up to three days [[80]].

Sunscreens are often used to protect the skin from solar UV radiation [[81]]. They contain absorbers, reflectors, and scatterers of UV light. Plant extracts [[82]] and other antioxidants [[83]] are also used to enhance skin protection [[84],[85]] and to increase the photo-stability of sunscreens [[86]].

5.2. Effect of Visible Light

Using in vivo RRS, Vandersee et al. [[87]] showed that the concentration of carotenoids in the human SC decreased by 13–21% after irradiation with light of the violet-blue spectral range (400–495 nm; dose 50 or 100 J/cm2: light intensity 100 mW/cm2, irradiation time 500 or 1000 s). A decrease in the carotenoid concentration was observed immediately after irradiation, and recovery to the initial value lasted between 2 up to 24 h, depending on the irradiation dose (50 or 100 J/cm2). It was suggested that violet-blue light causes ROS formation in the skin, which induces a decrease of the carotenoid concentration in the SC, was confirmed in an in vivo study of human skin using EPR spectroscopy [[88]] and in numerous studies evaluating oxidative stress-induced changes in the skin [[89],[90],[91]].

To protect the skin from the effects of radiation in the visible spectral range, the use of sunscreens that protect in the UV spectral range is ineffective. The incorporation of filters that absorb, reflect, or scatter light in the visible spectral range is rarely used in practice because visible light filters frequently have a dense texture and are not transparent, thus adding an undesirable color to the cosmetic product and, after application, to the skin [[92]]. Recent human skin studies in vivo demonstrated that topical application of sunscreens containing 0.005% Glycyrrhiza inflata root extract, namely the phenolic compound licochalcone A, has a protective antioxidant effect on human skin by neutralizing the violet-blue radiation-induced ROS [[93]]. Thus, the addition of antioxidants to cream formulations is effective in neutralizing ROS, which was also confirmed previously [[84],[90]].

5.3. Effect of Near-Infrared Radiation

The decrease of the carotenoid concentration in the human SC after irradiation with near-IR light (600–3000 nm; dose 306–342 J/cm2: light intensity 170–190 mW/cm2, irradiation time 30 min) was shown in vivo using RRS [[94]]. It was hypothesized that the decrease in the carotenoid concentration might be due to the neutralization of the formed ROS, and this assumption was later confirmed by a temperature-controlled ex vivo study on porcine skin using EPR spectroscopy [[95]]. These results were preceded by the work of Zastrow et al. [[96]], in which the free radical action spectrum of excised human skin was demonstrated—about 50% of free radicals (predominantly ROS) are formed in the skin by irradiation in the visible and near-IR spectral ranges. ROS are formed in the skin as a result of irradiation in the IR-A and IR-B spectral ranges, which is confirmed by the immediate decrease of carotenoid concentration in the SC after the termination of irradiation [[97]]. Recovery to the initial value lasted up to 24 h and starts in the superficial SC depth [[28]].

To protect the skin from IR-A and IR-B radiation, the use of absorbers, reflectors, and scatterers as part of sunscreens is less effective compared to protection in the UV spectral range. An effective protection includes the topical application of antioxidants (carotenoids) that neutralize IR-generated ROS [[98],[99],[100]].

5.4. Impact of Internal Stress Factors and Diseases

Using non-invasive RRS and diffuse reflectance spectroscopy it was shown in human skin in vivo that the consumption of high doses of alcohol [[101]], excessive physical activity [[102]], domestic and work stress [[22],[103],[104]], and other stress factors [[104],[105]] result in a reduction of the carotenoid concentration in the human SC. It has been noticed that the concentration of carotenoids in the SC of smokers is significantly lower than in non-smokers [[106],[107],[108]], which is in agreement with the literature data [[109],[110],[111]]. The concentration of carotenoids in the SC of women is significantly higher than in men [[108]] and tends to decrease with increasing body mass index to values >30, which is also consistent with published data [[110],[111],[112]].

It is known that various diseases can cause a disturbance of the redox balance, which leads to the development of oxidative stress that is accompanied by a decrease in the antioxidant concentration [[113],[114],[115]].

A number of studies have shown an association between a diet rich in carotenoids, e.g., fruit and vegetables, and the risk of developing certain types of cancer according to the following principle: the more carotenoids in a diet, the lower the probability of cancer development [[116],[117],[118]]. The same relationship has been observed between a carotenoid-rich diet and the risk of cardiovascular [[119],[120]], eye [[121]], and other diseases [[30],[122]]. The inverse relationship for the development of lung cancer has been reported for heavy smoking individuals after supplementation of a high single dose of ß-carotene, which strongly exceeds the physiological concentration [[123]].

It was shown that the concentration of carotenoids in the SC of various cancer patients measured before chemotherapy was significantly lower than that of healthy individuals [[124]], probably due to the psychological burden and anxiety that cancer patients suffered from or the accumulating long-lasting effect of previous chemotherapy cycles [[125]]. Although the concentration of carotenoids in the SC does not correlate with the age of a healthy person [[108]], such a correlation has been found for the skin of cancer patients, which was decreasing with increasing patient age [[126]].

Thus, it could be concluded that the action of internal stressors, including various diseases, leads to a decrease in the concentration of carotenoids in the SC, which entails a decrease of the entire antioxidant status.

5.5. Effect of Chemotherapy

Doxorubicine and its metabolites appeared within the sweat glands spreading continuously over the skin surface of palms and soles, which exhibit a high density of sweat glands. The fluorescent signal of doxorubicine could be detected 1–2 h after starting the intravenous infusion and remained there for at least 4.5 h [[127]]. Before the invention of targeted therapies and immune therapy, many common chemotherapeutic agents were based on or caused radical formation, e.g., cytostatics inducing in particular ROS, increasing the amount of oxidation products in the body [[128],[129]]. Cutaneous antioxidants neutralize part of the chemotherapy-induced free radicals and are further destroyed. Thus, the higher the concentration of antioxidants in the patient’s skin, the more effective the neutralization of free radicals and protective potential regarding skin toxicities.

A chemotherapy including intravenous infusion of paclitaxel (175 mg/m2 every 3-weeks), docetaxel (30–35 mg/m2 every 3-weeks), or 5-fluorouracil (2400 mg/m2 every 2-weeks), leads to a significant decrease of the carotenoid concentration in the palm immediately after a single infusion by ≈5, ≈12, and ≈7% on average, respectively, which is an indirect indicator of increased oxidative processes [[126]].

Thus, it has been shown, directly and indirectly, that systemically applied chemotherapeutic agents can reach the skin surface as part of the sweat, where they re-penetrate into the SC, interacting with its components, and reducing the carotenoid concentration [[124],[126]].

6. Factors Leading to An Increase of Carotenoids in the SC

As demonstrated earlier, the carotenoid concentration in the SC decreases as a result of different stress factors. On the other hand, there is always a compensatory effect—the restoration of the carotenoid concentration in the SC, which is considerably slower compared to the degradation process [[80],[87],[94],[101]] and strongly depends on nutrition and on the carotenoids that are stored in the body.

6.1. Effect of a Carotenoid-Rich Nutrition on the Carotenoid Concentration in the SC

In vivo studies on humans show that the controlled consumption of dietary carotenoid-containing supplements leads to a significant dose-dependent increase in the carotenoid concentration in the blood plasma (on average by 200%) and in the SC (on average by 25%) [[130],[131],[132],[133]]. The same effect is observed with the consumption of carotenoid-containing food, in particular fruit and vegetables [[134],[135],[136],[137],[138],[139]]. At the same time, the carotenoid concentrations in the blood plasma and in the SC are strictly correlated [[64],[67],[140],[141],[142],[143]]. Using RRS, it was shown in vivo that an 8-week course of daily oral intake of plant antioxidants including carotenoids, has a long-term effect of increasing the carotenoid concentration in the SC [[131]]. After finishing the intake, the carotenoid concentration in the SC is reduced to its initial value within 5-weeks, which exceeds the 2–4-weeks of the SC renewal. Therefore, it has to be assumed that the carotenoids saturate the SC by continuously diffusing from the storage in the body.

In a placebo-controlled randomized study using diffuse reflectance spectroscopy [[144]] in 29 healthy women of Fitzpatrick skin Type II [[145]], the daily oral supplementation of a green cabbage carotenoid-rich extract (1.65 mg carotenoids/day) shows a significant increase of the carotenoid concentration in the SC of the palm by ≈10–22%. In addition, a significant increase in the concentration of collagen I after 5- and 10-months of green cabbage extract supplementation was shown on the cheek (increase by ≈18 and ≈17%, respectively) and the inner forearm (increase by ≈20 and ≈12%, respectively) [[144]]. Thus, increased concentrations of carotenoids in the SC lead to slower degradation of collagen I and, probably, promote the production of new collagen I by fibroblasts.

6.2. Effect of a Carotenoid-Rich Nutrition on the Antioxidant Status of the SC

The intake of the verum carotenoid-rich supplement (4.45 mg carotenoids/day) within 4- and 8-weeks resulted in a significant increase in the carotenoid concentration in the SC [[107]], which is in agreement with previous results with a 4-weeks supplementation (9 mg carotenoids/day) [[132]]. A total of 12-weeks after the termination of the dietary supplementation, the carotenoid concentration in the SC had decreased to the initial level. In the placebo group the carotenoid concentrations in the SC did not significantly change over the total duration of the studyresearch. The rate constant k correlates with the carotenoid concentration: unchanged in the placebo group, increasing after 4- and 8-weeks in the verum group, and decreasing to the initial value 12-weeks after the intake termination. After an 8-week intake of the verum supplement, when the difference in the carotenoid concentration and antioxidant status in the SC was the highest between the two groups, all the volunteers were exposed to a sunlight simulator (420–2000 nm; dose 72 J/cm2: light intensity 120 mW/cm2, exposure time 10 min) to induce free radicals. The free radicals were recorded in vivo by EPR spectroscopy using the stable nitroxide spin probe PCA (3-carboxy-2,2,5,5-tetramethyl-1-pyrrolidine-1-oxyl), which does not react with antioxidants of the human epidermis [[5]]. The results show that the amount of free radicals generated in the SC is significantly lower (by ≈34%) in the verum than in the placebo group. This effect is related to the antioxidant property of carotenoids to neutralize free radicals, further confirming the increased antioxidant status of the SC in the verum compared to the placebo group. These results explain the reduction of the UV-B light-induced erythema intensity, which had been reported in other studies for the group of volunteers taking carotenoid supplements [[65],[101],[146]] and further support the conclusion that carotenoids can be considered as marker substances for the entire antioxidant status of the human SC in vivo [[73]]. Consequently, a diet that is enriched with carotenoids leads to an increase in their concentration in the skin, and also to an increase in the antioxidant status of the SC [[107]].

6.3. Effect of a Carotenoid-Rich Cosmetics on the Carotenoid Concentration in the SC

The fastest way to increase the concentration of antioxidants in the SC is the topical application of a cream containing antioxidants, which increases the skin protection against the effects of IR [[81],[84],[98],[99],[100]] and visible [[81],[84],[93],[98]] radiation. It was shown that the daily application of a cream containing antioxidants, including 0.2% carotenoids, for 8-weeks has a short-term effect. After termination of the cream application the carotenoid concentration in the SC is reduced to the initial value within 10-days [[131]]. It has been demonstrated that combined oral and topical application of carotenoids leads to the most efficient and prolonged (up to 5-weeks) increase in the concentration of carotenoids in the SC [[131]]. These results are in agreement with the current data in the literature [[111],[147]].

6.4. Biofeedback as Motivation for a Healthier Lifestyle

Diffuse reflectance spectroscopy was used twice a week for 7-months to investigate changes in the concentration of carotenoids in the SC of the palm in 50 high school students. Before starting the restudyearch, basement values of the cutaneous carotenoids were assessed. Afterwards, an intervention was conducted; the students received lectures on the importance of a healthy nutrition and lifestyle. Furthermore, the function of antioxidants and the factors influencing its change were explained, which subsequently served as a motivating factor for a healthier lifestyle. After each measurement a questionnaire was completed including an assessment of the amount of fruit and vegetables in the daily diet, the current subjective stress level (including social and personal stress, exams, lack of sleep), health status (illness, fatigue), smoking, and alcohol consumption. The results showed that the concentration of carotenoids in the SC significantly increased after the intervention was conducted [[148]].

Another important result of this restudyearch was the observation of an even competitive motivation for higher antioxidant values among the participants. Comparing their skin carotenoid values with each other, the students started to compete for higher concentrations, thus striving for a healthier lifestyle. The rapid and non-invasive feedback by their antioxidant values gave the participants additional motivation to take part in the studyresearch and to improve their dietary and lifestyle habits [[148]].

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