Bioresource Technology 184 (2015) 355–362

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Review

Exploring the potential of using algae in cosmetics

Hui-Min David Wang a,b, Ching-Chun Chen a, Pauline Huynh c, Jo-Shu Chang d,e,f,⇑
a
Department of Fragrance and Cosmetic Science, Kaohsiung Medical University, Kaohsiung 807, Taiwan
b
Graduate Institute of Natural Products, Kaohsiung Medical University, Kaohsiung 807, Taiwan
c
Ecole de Biologie Industrielle, École de Biologie Industrielle, 95094, France
d
Department of Chemical Engineering, National Cheng Kung University, Tainan 701, Taiwan
e
Center for Biosciences and Biotechnology, National Cheng Kung University, Tainan 701, Taiwan
f
Research Center for Energy Technology and Strategy, National Cheng Kung University, Tainan 701, Taiwan

h i g h l i g h t s

 Algae extract combats skin aging, de-pigmentation and anti-microorganism.

 Algae can be functional antioxidants, alginates, polysaccharides and carotenoids.
 Algae extract contributes skin health and beauty in practical cosmetic uses.

a r t i c l e i n f o a b s t r a c t

Article history: The applications of microalgae in cosmetic products have recently received more attention in the treat-
Received 4 September 2014 ment of skin problems, such as aging, tanning and pigment disorders. There are also potential uses in the
Received in revised form 30 November 2014 areas of anti-aging, skin-whitening, and pigmentation reduction products. While algae species have
Accepted 1 December 2014
already been used in some cosmetic formulations, such as moisturizing and thickening agents, algae
Available online 8 December 2014
remain largely untapped as an asset in this industry due to an apparent lack of utility as a primary active
ingredient. This review article focuses on integrating studies on algae pertinent to skin health and beauty,
Keywords:
with the purpose of identifying serviceable algae functions in practical cosmetic uses.
Algae
Skin aging
Ó 2014 Elsevier Ltd. All rights reserved.
Depigmentation
Antimicrobial functions
Cosmetic formulation

1. Introduction microbial antigens into antigen presenting cells by interacting with

T cells. Sebaceous glands produce an oily substance known as
1.1. Composition and function of the skin sebum that lubricates the skin, although the occlusion and infec-
tion of these can trigger acne (Zouboulis, 2004). Receptors in the
As the biggest organ in the human body, the skin has an impor- skin detect various environmental stimuli and respond accord-
tant role in many physical functions (Wang et al., 2013a,b). Skin is ingly, with mechanoreceptors detecting sensations and thermore-
composed of the epidermis, dermis and hypodermis. Generally ceptors detecting heat. These receptors can cause sweat glands to
speaking, the epidermis is subdivided into five separate strata: produce sweat, thus maintaining temperature homeostasis as well
basal, spinous, granular, lucid, and corneum, as shown in Fig. S1 as getting rid of waste (Denda et al., 2007). Insulation is also pro-
(supplementary materials). In the epidermis, the predominant vided in the subcutaneous layer of the skin, where fat is stored.
keratinocyte cells repair skin damage, while melanocytes contain Skin absorbs not only oxygen and water, but also certain drugs,
melanin, thus determining skin color and protecting the skin from such as topical steroids. In addition, skin is rich in 7-dehydrocho-
UV light (Brenner and Hearing, 2007). Langerhans cells, a type of lesterol, and when it is exposed to UV light this substance is con-
dendritic cell, provide a degree of immunity (Wollenberg et al., verted into vitamin D (cholecalciferol), which is otherwise
1996), as they take up microbial antigens in the skin and transform obtained by dietary means, such as by ingesting dairy products
(Chen et al., 2007).
⇑ Corresponding author at: 1, University Road, East District, Tainan City 701, The stratum corneum (SC) on top of the skin is an important
Taiwan. Tel.: +886 6 2757575x62651; fax: +886 6 2357146. barrier to passive water diffusion from the skin, preventing dehy-
E-mail address: changjs@mail.ncku.edu.tw (J.-S. Chang). dration and thus enabling humans to live in air (Cartlidge, 2000).

http://dx.doi.org/10.1016/j.biortech.2014.12.001
0960-8524/Ó 2014 Elsevier Ltd. All rights reserved.
356 H.-M.D Wang et al. / Bioresource Technology 184 (2015) 355–362

It is also a barrier to certain irritations to the skin. For example, the proteins, or immunologically effective and virostatic compounds
immune function of the skin prevents damage from UV light by the (Pulz and Gross, 2004).
use of pigmentation (Wickett and Visscher, 2006). Under the epi-
dermis is the dermis, which is mainly composed of connective tis- 1.4. Functions and industrial applications of algae
sues, including blood vessels sweat glands, nerves, fibroblasts,
collagen and elastin. Collagen and elastin, which are cross-linked, More than 70% of the earth is covered by ocean, which is home
provide support for the skin. Hyaluronic acid (HA) is also a major to up to 90% of the planet’s organisms. The ocean provides many
component of the dermis, where it is involved in tissue repair. unique environments and rich resources, and there are numerous
HA is of fundamental importance in water retention, and can marine organisms with great potential to produce bioactive com-
absorb water about 1000 times its own volume. Nevertheless, col- pounds that can be used as pharmaceuticals, nutraceuticals and
lagen and HA break down with aging, causing wrinkles to appear cosmeceuticals. Therefore, more research is necessary to explore,
and the skin to lose firmness. The third layer, the hypodermis, is identify, understand, and eventually make use of the organisms liv-
composed mainly of fat and a layer of loose connective tissue. It ing in the ocean (Gomez et al., 2009).
provides insulation to the body, storing energy, and mechanically Over the last 2.45 billion years, algae have adapted to extremely
allows the attenuation and dispersion of externally applied pres- harsh and competitive environments by producing an array of
sure (Benbow, 2009). compounds and secondary metabolites for chemical defense, and
are thus able to live in a wide range of ecological niches (Kelman
1.2. The cosmetics industry and consumer requirements et al., 2012). They can be found in all ecosystems, both in water
and on land, even in places that cannot grow crops, such as deserts
According to the definition of the Federal Food, Drug & Cosmetic and seashores. Algae are extraordinarily diverse within the
Act of the US FDA and article L5131-1 of the French Public Health domains of Eukaryotes and Eubacteria, and have had many highly
Code, a cosmetic product is any substance or preparation that is to complex interrelations among each other in their evolutionary
be rubbed, poured, sprinkled, or sprayed on, introduced into or paths. Among several major subgroups of Eukaryotes that can pro-
applied to external parts of the body, in particular the epidermis, duce energy by photosynthesis, algae are present in three out of
hair and capillary systems, nails, lips and external genitals, or to four. That is, many algae are mostly photosynthetic and have sim-
the teeth and the mucous membranes of the oral cavity as the ilar biological and ecological functions to those of plants (Stengel
product cleans, perfumes, protects them, modifies their appear- et al., 2011). Nevertheless, algae and plants do not share a common
ance, keeps them in good condition or helps to reduce body odors. evolutionary background, and their biochemistry differs signifi-
In short, it is a set of cosmetic procedures and treatments to reach cantly. To date, more than 20,000 species of algae have been
personal hygiene and beautification. Fig. S2 (supplementary mate- identified (Christaki et al., 2012), and they are responsible for
rials) shows the customer requirements for cosmetic products, about 40–50% of the photosynthesis that occurs on the planet each
which are that such items are safe, effective, protective, resilient, year, and contribute significantly to the mitigation of greenhouse
natural, and have good sensory quality. gas emissions (Qin et al., 2012). The size of marine algae ranges
The cosmetics industry has an estimated annual turnover of from microscopic individual cells of microalgae to much larger
US$170 billion according to the financial analysis reported by a organisms, called Macrocystis, that are more than 30 m long
French-based company – Eurostaf (Arora et al., 2012). The use of (Gomez et al., 2009).
cosmetics is driven by the pursuit of beauty, which a biological Microalgae are unicellular or simple multicellular species that
trait based on Darwinian principles. In much the same way that grow rapidly, living in harsh conditions and withstanding environ-
animals evolve certain visual features to attract, intimidate or pro- mental stressors, such as heat, cold, anaerobiosis, salinity, photo-
tect, humans engage in conscious manipulation of visual signals oxidation, osmotic pressure and exposure to ultra-violet radiation
using tools to achieve a similar functions. Etcoff et al. (2011) pro- (Christaki et al., 2012). Microalgae are superior to conventional
poses that features which are seen as composing a beautiful face plants in terms of productivity, limited seasonal variation, easier
are important biological signals of mate value, and suggests a pos- extraction and abundant raw materials (Christaki et al., 2012).
sible correlation with judgments of various social attributes, such They are cultivated in artificial batch, fed-batch and continuous
as attractiveness, competence, likeability, and trustworthiness. modes. Microalgae have considerable plasticity, making it possible
The most recent study of the world beauty market, carried out to use the same process for many different applications. For
by Eurostaf (Arora et al., 2012), indicate that cosmetic industry will instance, microalgae can be utilized for wastewater treatment, bio-
continue to grow, with one significant contributing factor being the fuels, food production, feed additives and chemicals. Moreover,
development of the middle classes in many emerging countries. microalgae can also transform solar energy and carbon dioxide into
However, despite this promising future, more research must be valuable biomass.
implemented to improve cosmetic products, and one area of inter- Macroalgae (seaweeds) can be found in coastal areas, and with-
est is the greater utilization of natural ingredients to achieve the out the organs that are common in terrestrial plants, they have
requests from customers. rather simple structures. Macroalgae can be divided into three
groups based on their dominant pigments: Chlorophyceae (green
1.3. The increasing need for natural and environmentally sustainable algae), Phaeophyceae (brown algae) and Rhodophyceae (red algae).
products Green algae can absorb a huge amount of light energy, while red
and brown algae cannot as they live in deeper waters where there
Recently, consumers become suspicious about chemical is insufficient sunlight. Brown algae account for approximately 59%
ingredient, and the need is back to fundamental or basic cosmetic of the total macroalgae cultivated in the world, followed by red
products. There is an increasing demand for natural and environ- algae at 40% and green algae at less than 1% (Christaki et al.,
mentally sustainable products, with, for example, extracts of mic- 2012). Macroalgae can be cultivated on seashores on a large scale.
roalgal biomass having a significant market value in this regard. Their growth rate is relatively rapid, and it is possible to control the
Researchers have found that marine algae-derived compounds production of their bioactive compounds such as proteins, poly-
can be utilized as cosmeceuticals. For example, phylogenetically phenols and pigments by manipulating the culture conditions
archaic cyanobacteria produce substances that exhibit antioxida- (Christaki et al., 2012). Investigations indicate that metabolites
tive effects, polyunsaturated fatty acids (PUFA), heat-induced derived from brown algae, such as phloroglucinol, can have
 H.-M.D Wang et al. / Bioresource Technology 184 (2015) 355–362 357

anti-inflammatory, anti-tumor, and anti-diabetic properties, as can be seen in the skin of newborns, young adults, and older indi-
well as aid in neuroprotection and the treatment of bone-related viduals. Progerin, a truncated version of the lamin A protein, works
diseases (Thomas and Kim, 2013). Another Phlorotannin that has with telomeres to trigger cellular senescence in normal human
been isolated from algae, phlorofucofur-oeckol-B, has inhibitory fibroblasts (Robert et al., 2009; Reddy and Comai, 2012;
effects on the release of histamine from rat basophile leukemia Nikolakis et al., 2013). Progerin accumulates over time as the skin
(RBL)-2H3 cells (Wang et al., 2009). A blue-green alga called Spiru- ages, and thus progerin expression is greater in older fibroblasts
lina has components that exhibit antihypertensive effects. than in younger ones (Takeuchi and Rünger, 2013). An extract from
The application of algae based on their valuable bioactive chem- an edible seaweed, called Alaria esculenta, has been shown to
ical constituents has gained considerable attention in recent years, induce a significant decline in the amount of progerin in aged
with applications in areas such as food, medicine, cosmetics, aqua- fibroblasts at the lowest tested concentration, although this inhib-
culture and horticulture. In addition, diatoms are also applied in itory effect was not observed in younger cells (Verdy et al., 2011).
nanotechnology, optical systems, semiconductor nanolithography Extrinsic aging results from exposure to UV radiation and
and drug delivery, and have the benefits of being widely available, related irritation, and is characterized by deterioration of the der-
with a massive diversity among species (Pallela et al., 2010). On the mal extracellular matrix (ECM) and keratinocyte dysplasia in the
other hand, algae have also been examined for use in the treatment epidermis, resulting in wrinkles, laxity, coarseness and mottled
of wastewater from greenhouses. For example, Hultberg et al. pigmentation (Kim et al., 2013). UV light is divided into UVA,
(2013) collected the drainage solution from a greenhouse and used UVB, and UVC. UVA can penetrate down through the dermis, and
it to grow Chlorella vulgaris and other indigenous algae, in order to not only induces the formation of wrinkles, but also triggers
assess their viability for use in wastewater treatment and recy- skin-related symptoms. UVB is more carcinogenic, and causes the
cling. The results showed observed that the concentrations of both skin to turn red and burn at a rate that this 1,000 times faster than
nitrogen and phosphorus were significantly reduced after such that seen with UVA. On the other hand, UVC is blocked by the
treatment. ozone layer, and thus poses no threat to the skin (Matsumura
The market for so-called functional foods is one of the most and Ananthaswamy, 2004; Hussein, 2005; Gomez et al., 2009).
dynamic segments in the food industry, especially with regard to
beverages and pharmaceuticals (Matthyssens et al., 2008; 2.1. Photo-protectivity and antioxidant capacity of algal extracts and
Bigliardia and Galatib, 2013). Marine algae are suitable for use as compounds
a nutritional supplement due to their broad range of useful chem-
ical properties (Behrens, 1999). Algal biomass can also be produced Skin naturally possesses antioxidant agents able to block reac-
in the forms of powders, tablets or capsules for easy consumption, tive oxygen species (ROS) and avoid cell destabilization (Masaki,
and thus more rapid acceptable by consumers. Commercial appli- 2010). However, these defenses can be overrun when the amount
cations of this are now dominated by four strains: Arthrospira, of ROS is increased by UV exposure. The resulting oxidative stress
Chlorella, Dunaliella salina and Aphanizomenon flos-aquae can lead to free radical cell damage, particularly to proteins and
(Spolaorea et al., 2006). lipid membranes, as well as DNA breakdown. ROS can also induce
Arthrospira is a valuable foodstuff because it is rich in protein cell death via apoptotic or necrotic processes, and this is clearly
and other nutrients, and has been shown to aid in the alleviation noticeable with the presence of wrinkles and skin dryness. ROS
of hyperlipidemia, suppression of hypertension, protection against accumulation may thus be responsible for photoaging complica-
renal failure, promotion of intestinal Lactobacillus, and suppression tions, such as cutaneous inflammation, melanoma and skin cancer
of elevated serum glucose levels. Chlorella contains b-1,3-glucan, (Pallela et al., 2010). Vitamins and various plant extracts have been
which is an active immunostimulator, a free-radical scavenger shown to possess potent antioxidative properties, and have been
and a reducer of blood lipids (Iwamoto, 2004), and thus has been widely used for skin care and protection, either as nutritional sup-
used as a food additive. D. salina is exploited for its b-carotene con- plements or for topical application (Nichols and Katiyar, 2010;
tent, which makes it an important ingredient of many dietary sup- Wang et al., 2013a,b). In addition to vitamins and plant extracts,
plements and functional foods. The other major commercial strain polysaccharides like laminaran, fucoidan and alginate derived from
is A. flos-aquae, which can be used alone or with other nutraceuti- brown algae, such as Fucus vesiculosus and Turbinaria conoides, also
cals and natural food products to promote human health have antioxidative properties (Jea et al., 2009), and can be applied
(Benedetti et al., 2004; Spolaorea et al., 2006). A number of second- to prevent skin aging and cutaneous disorders. Additionally, anti-
ary metabolites derived from algae are known for their benefits to oxidants can help to maintain the organoleptic properties of cos-
the skin. For example, an extract from Arthrospira can repairs the metic products by inhibiting lipid oxidation, thus avoiding changes
signs of early skin aging, exerts a tightening effect, and prevents in appearance, odor and flavor. Researchers have also found that
stria formation; while an extract from C. vulgaris stimulates colla- the red algae Porphyra umbilicalis contains large amounts of
gen synthesis in the skin, supporting tissue regeneration and wrin- mycosporine-like amino acids (MMAs) that can absorb UV light,
kle reduction (Stolz and Obermayer, 2005). Cosmeceuticals that and thus act as sunscreen (Shick and Dunlap, 2002).
contain microalgae or their extracts are thus in great demand,
especially when combined with other antioxidants or bioactive 2.2. Matrix metalloproteinase (MMP) inhibition and reduction of
chemicals, with one area of growth being in products to protect collagen degradation
the skin from sun-related damage (Pulz and Gross, 2004).
The matrix metalloproteinases (MMPs) are a family of structur-
ally and functionally related zinc endopeptidases capable of digest-
2. Algae against skin aging ing ECM components such as collagens, proteoglycans, fibronectin
and laminin, both in vitro and in vivo. They are strongly linked to
Skin aging is a slow, complex process of intrinsic and extrinsic the connective tissue remodeling processes associated with
aging (Yaar, 2006). Aging of skin causes many changes, including embryonic development, pregnancy, growth and wound healing
thinning, dryness, laxity, fragility, enlarged pores, fine lines and (Bodea et al., 1999). As noted earlier, UVB and UVA induce the for-
wrinkles. Intrinsic aging refers to degradation of the skin, in terms mation of ROS, which have the potential to activate blood neutro-
of greater prominence of vasculature, an increase in transparency, phils and induce elastin dystrophy. Neutrophils can infiltrate the
quality and loss of elasticity. It is reflected in the differences that skin to secrete neutrophile elastases, in turn activating MMPs.
358 H.-M.D Wang et al. / Bioresource Technology 184 (2015) 355–362

MMPs, particularly MMP-2 and MMP-9, degrade collagens and macrophages are viable even if they are treated with high concen-
elastic fibers, inducing loss of skin elasticity, promoting wrinkle trations of sargachromanol E. compound, and that there is no risk
formation, and accelerating skin aging, as indicated in Fig. S3 of cytotoxicity (Lee et al., 2013). Furthermore, morphological cell
(supplementary materials) (Inomata et al., 2003; Pillai, 2005; examinations under a microscope revealed normal elongated
Brenneisen et al., 2002). The central role of the activator protein fibroblasts with contact inhibition in confluence. In another exper-
1 (AP-1) transcription factor in transcriptional regulation of iment, inhibition of ROS generation was observed after cell UVA
MMP-1 is important (Joe et al., 2006). Previous studies have shown irradiation and treatment with sargachromanol E., and thus the
that the cooperation of AP-1 with nuclear factor j-light-chain- formation of intracellular ROS decreased. Sargachromanol E. treat-
enhancer of activated B cells (NF-jB) is essential for full activation ment has also been shown to inhibit lipid peroxidation, and the
of MMP-1 transcription. Thus, the functional components inhibited results of all these studies suggest that sargachromanol E. obtained
AP-1 and NF-jB, thereby suppressing the expression of MMP-1. Joe from S. horneri may be effective if applied in cosmetics to prevent-
et al. (2006) reported 15 seaweed extracts having the potential to ing photoaging of the skin. Moreover, fucosterol, a natural sterol
inhibit NF-jB or Ap-1 proteins, and the extracts from Ecklonia compound isolated from marine brown algae, has been reported
stolonifera (Alariaceae) showed both high 76.0% and 66.7% inhibi- to possess antioxidant and anticancer properties (Lee et al.,
tory effects on NF-k B and AP-1 reporter activity, respectively. 2003). A recent study showed that the viability of human keratino-
These results suggest that seaweeds in Alariaceae have more cytes cell (HaCaT) was not affected when cells were irradiated with
potent inhibitory effect on NF-j B and AP-1 reporter activity than UVB when incubated with concentrated fucosterol for 24 h. In
seaweeds in other families. addition, fucosterol treatment on HaCaT markedly decreased
Algae produce a wide variety of secondary metabolites with UV-irradiated MMPs production and expression, increasing type-I
many different biological activities. Fucoidan derived from brown procollagen production (Kim et al., 2013).
algae have recently been shown to inhibit UVB-induced MMP-1
expression in vitro by the suppression of extracellular signal regu-
lated kinase (ERK) (Thomas and Kim, 2013). Similarly, another
study by the same author reported that 16 kDa fucoidan could sup- 3. Skin whitening
pressMMP-3 induction on dermal fibroblasts in vitro (Thomas and
Kim, 2013). In addition, ex vivo studies of 16 kDa fucoidan using Skin whitening is a common practice all over the world, partic-
the human skin tissue have shown that it can minimize human ularly in Asia (Li et al., 2008). This is because white skin is seen as
leukocyte elastase activity, resulting in protection of the skin’s beautiful in Asian culture, and thus skin whitening products
elastic fiber network against enzymatic proteolysis. The results of account for a large share of the cosmeceutical market in this
these earlier works indicate that seaweed fucoidans could have region, with strong growth expected in the future. Tyrosinase cat-
great potential in reducing the risk of some inflammatory patholo- alyzes two distinct significant reactions in melanin synthesis: the
gies that involves extracellular matrix degradation by MMPs. hydroxylation of L-tyrosine to 3,4-dihydroxy-L-phenylalanine
Marine brown algae-derived phlorotannins, namely dieckol and (L-dopa) and the oxidation of L-dopa to dopaquinone, followed with
1-(30 ,50 -dihydroxyphenoxy)-7-(20 ,40 ,60 -trihydroxyphenoxy) 2,4,9- further conversion to melanin. Sun exposure increases the synthe-
trihydroxydibenzo-1,4,-dioxin, have been reported to suppress sis of both tyrosinase and melanosomes. Melanosomes mature to
both the protein and gene expression levels of MMP-1, MMP-3, form melanin, which then migrates to keratinocytes where degra-
and MMP-13 in human osteosarcoma cells (MG-63). They are also dation occurs to promote skin melanisation and tanning. The loss
able to inhibit ROS and block cytokine (Thomas and Kim, 2013). In of melanin by desquamation can then remove the tan (Fig. S4, sup-
addition, the report indicated that these phlorotannins can pro- plementary materials). The use of tyrosinase inhibitors is the most
mote osteosarcoma differentiation through collagen synthesis. common approach for skin whitening, as the enzyme catalyzes the
Likewise, dieckol and eckol isolated from E. stolonifera have inhib- rate-limiting step of pigmentation (Wang et al., 2011). In spite of
ited the expression of MMP-1 in human dermal fibroblast cell, the large number of in vitro tyrosinase inhibitors that have been
in vitro. More specifically, this earlier study suggested that these found, only a few have been shown to have any significant effects
phlorotannins interfered with the expression of NF-jB that con- in clinical trials (Thomas and Kim, 2013).
trols the transcription of DNA, and with activator protein-1 (AP- Marine algae have recently attracted attention in the search for
1), resulting in the enhancement of MMP-1 expression (Thomas natural tyrosinase inhibitor agents. Fucoxanthin isolated from
and Kim, 2013). Laminaria japonica has been reported to suppress tyrosinase
Corallina pilulifera (CP) belongs to the family Corallinaceae that activity in UVB-irradiated guinea pigs and melanogenesis in
is distributed throughout the coastal areas of the world. According UVB-irradiated mice (Thomas and Kim, 2013). Oral treatment with
to a study by Ryu et al. (2009), C. pilulifera methanol (CPM) extract fucoxanthin also suppressed skin mRNA expression linked to
attenuated MMP-2 and MMP-9 expression in HT-1080 cells, and melanogenesis, suggesting that fucoxanthin negatively regulates
treatment with CPM could significantly inhibit both MMP-9 and melanogenesis at the transcriptional level (Thomas and Kim,
MMP-2 expression in a dose dependent manner (Ryu et al., 2013). Phloroglucinol derivatives, another common secondary
2009). Sargachromanol E. is extracted from Sargassum horneri, a metabolite constituent of brown algae, also have tyrosinase inhib-
marine brown algae grown in the Sea of Japan and Korea. S. horneri itory activity due to their ability to chelate copper (Babitha and
has demonstrated anabolic effects with regard to bone calcification Kim, 2011). These studies suggest that bioactive compounds
both in vitro and in vivo, indicating that sargachromanol E. should derived from marine algae have a good potential to be utilized as
be further evaluated for its potential anti-aging effects. skin whitening agents. Kang et al. (2004) extracted seventeen sea-
Gomez et al. (2009) reported that fibroblasts treated with sarga- weeds to identify their tyrosinase inhibitory activity and applied
chromanol E. exhibited efficient protection against UVA induced L-tyrosine as the substrate in mushroom tyrosinase model.
collagen degradation, with this process inhibiting MMP expression E. stolonifera OKAMURA (Laminariaceae) was the only brown algae
in UVA irradiated dermal fibroblasts. The results showed that MMP that demonstrated the effective tyrosinase inhibition activity. The
levels were down-regulated by TIMP1 and TIMP2 after treatment authors further purified five compounds with bioassay-guided
with sargachromanol E., and the effect was higher than when fractionation of the functional ethyl acetate soluble fraction from
TIMP1 and TIMP2 were treated with retinoic acid. It has also been the methanolic extracts. Kang et al. (2004) also presented
observed that lipopolysaccharide (LPS) stimulated RAW 264.7 the phloroglucinol derivatives inhibitory mechanisms with
 H.-M.D Wang et al. / Bioresource Technology 184 (2015) 355–362 359

Lineweaver–Burk plot method to point out the possible competi- hair conditioners, and wound-healing agents, and can also mois-
tive and noncompetitive suppression reactions in pigmentation. turize, hydrate, emulsify, and emolliate (Goddard and Gruber,
1999).
4. Antimicrobial properties of seaweed extracts
5.1. Application of algae as moisturizing agent
The antimicrobial properties of seaweeds have been known
It is widely recognized that moisturization is the first step in
since ancient times and well-documented in recent years
acting against aging of the skin (Bonté, 2011), helping to maintain
(González del Val et al., 2001; Patra et al., 2008). , and thus they
its appearance and elasticity, while also strengthening its role as a
are of interest for potential use in cosmetic products. Seaweeds
barrier to harmful environmental factors. Corneocytes, hyaluronic
have the ability to kill fungi and bad bacteria, maintaining skin
acid and regulated water transport within the skin all work to
flora in state of balance (Fig. S5, supplementary materials). They
retain moisture inside the human body. Recent research revealed
can thus act as preservatives to prevent the growth of such organ-
that water and glycerol transport proteins, named aquaporins,
isms, which may spoil the cosmetics or even harm users (Vilchez
combine with corneodesmosomes and tight junctions to enable
et al., 2011). For example, four species of Algerian marine algae
the movement of water between cells in different layers of the epi-
were tested for their anti-fungi properties, and the results showed
dermis, therefore moisturizing the skin (Bonté, 2011). Water and
that that they had fungi-inhibiting effects, among which Rhodomel-
pH regulate the epidermal enzymes associated with corneocyte
a confervoides (red algae) and Padina pavonica (brown algae) were
desquamation and lipid synthesis. Furthermore, the level of skin
the most effective against Candida albicans and Mucor ramaniannus,
moisturization is strongly linked to its defense of irritant agents
respectively, which are the two major groups of microorganisms
or frequent washing with strong tensioactive materials.
that can be found on the skin (Saidani et al., 2012). Some of the
Cosmetic formulations containing hydroxy acid (HA) have been
Candida albicans, namely probiotics, can protect the skin while
used in clinical practice to moisturize the skin. HA can be found in
Mucor ramaniannus will cause infections and diseases (Noble,
plants and animals, but since the supply of HA is limited, the price
1975). For instance, pregnant women or people using antibiotics
is relatively high. In contrast, polysaccharides derived from algae
may have unbalanced skin flora, resulting in skin contamination.
are abundant and environmental-friendly raw materials, which
Staphylococcus aureus is part of the human flora, and is primar-
are relatively cheap and can be used as substitutes for petrochem-
ily found on many skin surfaces, such as those of the nose, mouth,
icals. A study conducted by Wang et al. (2013a) and Wang et al.,
genital and anus. Although these bacteria are generally harmless,
2013b showed that polysaccharides extracted from Saccharina
when the skin is punctured or broken for any reason staph bacteria
japonica, a type of brown algae, absorbed and retained more mois-
can enter the wound, causing infections that range from self-limit-
ture than polysaccharides extracted from four other species of
ing to life-threatening. S. aureus is gram-positive, and many of
algae, and particularly when there was a decrease in molecular
staphylococcus strains produce staphylococcal enterotoxins, super-
weight, with only one sample of the algal polysaccharides being
antigen toxic shock syndrome toxin (TSST-1), and exfoliative tox-
an exception to this. The study also indicated that polysaccharides
ins. When these toxins are secreted on the epidermis they can
extracted from S. japonica performed better than HA with regard to
cause blisters, skin loss, pimples, furuncles, impetigo, folliculitis,
moisturization, suggesting that algae-derived polysaccharides
abscesses, poor temperature control, fluid loss, secondary infec-
could be used as an additive in cosmetics. Chondrus cripus is a
tion, and scalded skin syndrome, among other conditions (Lowy,
red algae abundant in polysaccharides and minerals that have
1998). Laurinterol derived from the red algae Laurencia pacifica
hydrating, therapeutic and moisturizing effects. An extract from
can be applied to treat infections due to S. aureus (Fenical, 1976),
green algae, Codium tomentosum, can regulate water distribution
with one study finding that it achieved complete inhibition within
in the skin, and thus protect the skin from dryness, particularly
48 h after inoculation, and at concentrations comparable to those
in dry environments. Moreover, DNA extracted from algae or other
of streptomycin (Sims et al., 1974). Plaza et al. (2010) developed
marine organisms can be utilized for skin moisturization and pro-
a novel screening method with the pressurized liquid extraction
tection, including extracts from Undaria pinnatifa, Durvillea antarc-
to examine the anti-microorganisms abilities. By using this assay,
tica, Ascophyllum nodosum, Cladosiphon okamuranus, Pediastrum
it becomes possible to examine the functional components within
duplex and Polysiphonia lanosa. An extract from Chlorella vulgaris
an alga, Himanthalia elongata, and a microalga, Synechocystis sp.
is another promising substance for use in skin care products, as
They showed two algae antimicrobial activities with various pres-
it boosts collagen synthesis, supporting skin tissue and thus reduc-
surized liquid extraction temperatures on four microorganisms,
ing wrinkles.
Escherichia coli, S. aureus, Candida albicans and Aspergillus niger.
The variations among the experiment solvents presented a thought
5.2. Use of algae as a thickening agent
of the main components discovered within both algae samples to
show their anti-microorganism properties.
A number of ingredients are used for the thickening purpose
resulting from a general requirement to control viscosity to pro-
5. Use of algae in cosmetics duce an appealing liquidity in cosmetic products. Alginic acids,
which are polysaccharides isolated from brown algae and bacteria,
There are many polysaccharides that can be used in cosmetics, are good hydrocolloids that can be used to thicken and stabilize
with different morphologies and functions. Polysaccharides in emulsions. Thus they can be applied in many cosmetic products
solution can exist in the form of loose random coils or rigid helices. (Sachan et al., 2009; Priyadarshani and Rath, 2012). These are com-
They can be anionic, cationic, nonionic, or amphoteric, depending posed of two different monosaccharides, b-d-(1,4)-mannuronic
on their chemical identity, as expressed in their native structure, acid and a-l-(1,4)-guluronic acid, which can be extracted using
which can be influenced by temperature, concentration, and the alkali and subsequent treatment with mineral acids. Alginic acids
presence of other species. Marine algae are the most abundant absorb water quickly and provide cellular support to keep the cells
source of natural polysaccharides, such as fucoidans derived from of brown algae and bacteria from collapsing, and this is the basis of
brown algae, carrageenans from red algae and ulvans from green their use in cosmetic formulations (Wijesinghe et al., 2011). Agar is
algae. Polysaccharides have a large number of cosmetic functions. another polysaccharide that can be applied as a thickener to con-
For example, they act as rheology modifiers, suspending agents, trol both viscosity and emollience in cosmetic products, with agar
360 H.-M.D Wang et al. / Bioresource Technology 184 (2015) 355–362

extracted from red algae, such as Pterocladia, Pterocladiella and Gel- melanin and improve the condition of all skin layers via both top-
idium, being of especially high quality. Nevertheless, more than ical and oral use (Tominaga et al., 2012). Fucoxanthin is the main
50% of agar is now produced from Gracilaria gracilis and Gracilaria carotenoid present in the chloroplasts of brown algae, such as Cer-
chilensis instead. cis siliquastrum, Undaria pinnatifida, Sargassum fulvellum, L. japonica
When a polyvalent cation causes interpolysaccharide binding, a and H. fusiformis. It is estimated that fucoxanthin accounts for
junction zone occurs in the cross-linking sites. The calcium ion, in more than 10% of the total production of natural carotenoids
particular, has been widely studied for its ability to form junction (Christaki et al., 2012). It has the ability to counteract oxidative
zones in alginate solutions. At least two L-guluronic acid residues stress caused by UV radiation, and thus is applicable for use in cos-
need to be sequential in the chain to form these zones, with much meceuticals (Wijesinghe et al., 2011). Maeda et al. (2005) sug-
higher numbers needed to form strong junction zones. As the con- gested that fucoxanthin enhanced the fat burning rate of fat cells
centration of the polyvalent cation increases, the viscosity of the in the adipose tissue due to an increase in thermogenin. Microalgal
liquid solution also rises and eventually become gel-like. Further b-carotene, known to be a vitamin precursor, is one of the leading
addition of calcium will cause alginic acid to precipitate in the food colorants, produced mainly from Dunaliella spp. or from Spiru-
solution. Cosmetic formulations that apply alginates must control lina platensis (Pulz and Gross, 2004; Prasanna et al., 2007). b-Car-
the polyvalent metal ion concentrations through the use of seques- otene also has a strong antioxidant capacity, which helps to
trants, such as ethylenediaminetetraacetic acid (EDTA), to optimize counteract the free radicals involved in gastrointestinal cancer,
thickening effects. PH is another factor that influences the viscosity arthritis or premature aging. Lutein is an intracellular algal product
of alginate solution, with most anionic polysaccharides affected by found in Scenedesmus and Chlorella (Sánchez et al., 2008), and has
changes in pH. The effect of pH on alginates is most noticeable near been found in the epidermal and dermal layers, protecting the skin
pH 4, and below this the viscosity increases very rapidly, while from UV-induced damage, particularly when combined with other
above pH 10 the solution becomes unstable. In other words, algi- antioxidants, and immunoprotective substances. The lutein and
nate solution should not be used at either pH extreme. zeaxanthin found in algae such as Rhodophyta spp. and Spirulina
Carrageenans are polysaccharides that have been isolated from spp. are often applied in food coloring, drug and cosmetics
red algae, with at least seven varieties discovered to date. These (Hallmann, 2007). Reports indicate that lutein plays an active role
substances are fairly functional, as they are anionic substituents. in preventing acute and chronic coronary symptoms, maintaining
A thermal stimulus is required for carrageenan to form a double normal visual functions, hindering the development of cataracts,
helix, since this process is temperature dependent. The polymer stimulating the immune response, delaying progression of early
chains exist as random coils following initial dissolution of the atherosclerosis, avoiding gastric infection and inhibiting macular
polysaccharide in hot water. When cooled down, the polysaccha- degeneration linked to age (Vilchez et al., 2011; Yaakob et al.,
ride chains gather together and eventually form a double helix, 2011). Despite the many benefits of lutein, as yet there is a lack
which facilitate the formation of further junction zones in the pres- of mass production on a commercial scale, although efforts are
ence of various cations under the influence of the anionic sulfate now underway to establish the outdoor production of microal-
groups, creating interhelical cross-links that cause higher solution gae-based lutein (Yaakob et al., 2011).
viscosity, and eventually gelation. Lambda-carrageenan is another
polysaccharide that produces viscosity through random chain
6. Conclusion
entanglement. In addition to being temperature sensitive, the rhe-
ological effect of kappa-carrageenan also relies on the molecular
Algae are rich-sources of structurally novel and biologically
weight. Specifically, rises in viscosity are accompanied by increases
active metabolites, with great industrial potential and accessibility,
in its molecular weight (Goddard, 1999).
and thus they have attracted attention for health and cosmetic
applications. This review examines the use of microalgae, macroal-
5.3. Application of algae as pigmenting agent: carotenoids
gae and their derivatives in applications to combat skin aging, as
well as for depigmentation and antimicrobial applications in the
There is now increasing demand for natural pigments derived
cosmetic industry. A wide range of metabolites, such as antioxi-
from carotenoids, rather than those that are chemically synthe-
dants, anti-inflammatory agents, alginates, polysaccharides,
sized, as the latter are suspected of being carcinogenic, inflecting
carotenoids, and so on, have been investigated for cosmeceutical
damage on the liver and kidneys. The price of natural pigments iso-
preparations. Algae are thus a source of raw materials for one of
lated from algae can be as much as 700 Euros per kilo, more than
the most promising and profitable sectors of the biotechnology
double that of synthetic products (Guedes et al., 2011). The Chloro-
industry.
phyceae family, including Dunaliella, Muriellopsis, Chlorella and
Haematococcus, is the most common source of these, as it tends
Acknowledgements
to accumulate carotenoids within its own biomass (Guedes et al.,
2011). Carotenoids are isoprenoid molecules, responsible for the
This work is financially supported by Taiwan’s National Science
color of fruits, vegetables, and flowers, as well as some birds,
Council under Grant Nos. 102-2811-E-006-058, 102-2622-E-011-
insects and marine animals. They can be divided into carotenes
001-CC2, NSC102-2622-E-037-002 and MOST 103-2221-E-037-
and xanthophylls. Some xanthophylls can be synthesized by mic-
004, and Taiwan’s Bureau of Energy, Ministry of Economic Affairs.
roalgae, while others can be derived from brown algae. Carotenoids
We also thank the project of Center for Stem Cell Research, Kaoh-
are used in foods as a natural color enhancer, as well as in the phar-
siung Medical University, KMU-TP103G00 and KMU-TP103G02-05.
maceuticals and cosmetic industries (Ye et al., 2008; Vichez et al.,
The authors also thank Mr. Jung-Chien Wu of University of British
2011).
Columbia, Canada for his contribution to this article.
Astaxanthin is the main carotenoid found in Haematococcus plu-
vialis. It is an excellent antioxidant, more powerful than vitamins C
and E or other carotenoids, while preserving the proteins and Appendix A. Supplementary data
essential lipids of human lymphocytes due to its superoxide
dismutase and catalase enzyme activities (Bolin et al., 2010; Supplementary data associated with this article can be found, in
Vilchez et al., 2011; Pan et al., 2012). It has been reported that asta- the online version, at http://dx.doi.org/10.1016/j.biortech.2014.
xanthin can suppress skin hyper-pigmentation, inhibit synthesis of 12.001.
 H.-M.D Wang et al. / Bioresource Technology 184 (2015) 355–362 361

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