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Wageningen 

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Beneficial Microbes, 2014; 5(2): 99-107 P u b l i s h e r s

Impact of prebiotics and probiotics on skin health


http://www.wageningenacademic.com/doi/pdf/10.3920/BM2013.0040 - Thursday, September 21, 2017 1:35:57 AM - Göteborgs Universitet IP Address:130.241.16.16

F.H. Al-Ghazzewi and R.F. Tester

Glycologic Limited, 70 Cowcaddens Road, Glasgow, G4 0BA, United Kingdom; f.h.alghazzewi@glycologic.co.uk

Received: 24 September 2013 / Accepted: 8 December 2013


© 2014 Wageningen Academic Publishers

REVIEW ARTICLE
Abstract

This review discusses the role of pre- and probiotics with respect to improving skin health by modulating the
cutaneous microbiota. The skin ecosystem is a complex environment covered with a diverse microbiota community.
These are classified as either transient or resident, where some are considered as beneficial, some essentially neutral
and others pathogenic or at least have the capacity to be pathogenic. Colonisation varies between different parts of
the body due to different environmental factors. Pre- and probiotic beneficial effects can be delivered topically or
systemically (by ingestion). The pre- and probiotics have the capacity to optimise, maintain and restore the microbiota
of the skin in different ways. Topical applications of probiotic bacteria have a direct effect at the site of application
by enhancing the skin natural defence barriers. Probiotics as well as resident bacteria can produce antimicrobial
peptides that benefit cutaneous immune responses and eliminate pathogens. In cosmetic formulations, prebiotics
can be applied to the skin microbiota directly and increase selectively the activity and growth of beneficial ‘normal’
skin microbiota. Little is known about the efficacy of topically applied prebiotics. Nutritional products containing
prebiotics and/or probiotics have a positive effect on skin by modulating the immune system and by providing
therapeutic benefits for atopic diseases. This review underlines the potential use of pre- and probiotics for skin health.

Keywords: prebiotic, probiotic, synbiotic, skin microbiota, skin health

1. Introduction redefined the concept as ‘A live microbial feed supplement


which beneficially affects the host animal by improving
Recently, attention has grown regarding the use of pre- and its intestinal balance’. Havenaar and Huis in’t Veld (1992)
probiotics in the cosmetic fields. Firstly, to manipulate proposed a similar definition as ‘a viable mono or mixed
the compositional and/or functional properties of culture of bacteria which, when applied to animals or man,
skin microbiota. Secondly, to contribute towards skin beneficially affects the host by improving the properties
regeneration and blemish/wound healing. This review of the indigenous flora’. A commonly cited definition is
discusses the role of pre- and probiotics in cosmetic ‘live microorganisms, which when consumed in adequate
products and the associated scientific underpinning. amounts, confer a health effect on the host’ (FAO/WHO,
2001). Probiotic bacteria strains belonging to the genera
Body friendly bacteria – ‘probiotics’ Bifidobacterium and Lactobacillus are the most common
probiotics, although other species from other bacterial
The term probiotic means ‘for life’ and it is used to name genera such as Bacillus, Enterococcus and Streptococcus,
microorganisms associated with beneficial effects in in addition to the yeast Saccharomyces, have also been
humans and animals (FAO/WHO, 2001). A number of classified as probiotics (Boyle et al., 2011).
definitions have been proposed for this concept, going back
to 1907, when the Russian immunologist Eli Metchnikoff Probiotic efficacy is concerned traditionally with the gut of
defined it as ‘The dependence of the intestinal microbes the host (especially colon). In terms of applications to the
on the food makes it possible to adopt measures to modify skin, the beneficial effect can be achieved (1) by ingesting
the flora in our bodies and to replace the harmful microbes the live microorganisms (Levkovick et al., 2013) or (2) by
by useful microbes’ (Metchnikoff, 1907). Fuller (1989) topical applications (Di Marzio et al., 2008; Farmer and

ISSN 1876-2833 print, ISSN 1876-2891 online, DOI 10.3920/BM2013.004099


F.H. Al-Ghazzewi and R.F. Tester

Mikhail, 1998; Krutmann, 2009; Volz and Biedermann,


2009). Probiotics have the capacity to optimise, maintain Prebiotics
and restore the microbiota of the skin in different ways. Act as nutrient
However, the application of live probiotics to the skin sources
creates many challenges (Tester and Al-Ghazzewi, 2012).
Probiotics
These relate to ensuring the viability of probiotic bacteria Topical
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and being able to recolonise the skin after the addition applications Ingestion
of new microbiota, which may themselves be a harsh
environment. Unbalanced skin microbiota
P. acnes > S. epidermidis
Selective nutrition for probiotics – ‘prebiotics’ Promote the growth of Gastrointestinal
beneficial microbiota at tract
the expense of harmful
In contrast to probiotics, a prebiotic is defined according microbiota
to the classical view of Gibson and Roberfroid (1995) and Systemic
Roberfroid (2007) as ‘a selectively fermented ingredient Balanced skin microbiota effects
that allows specific changes, both in the composition S. epidermidis > P. acnes
and/or activity in the gastrointestinal microflora that
confers benefits upon host well-being and health’. The Help prevent skin
term prebiotic was developed initially to describe materials diseases
(carbohydrates) which travel to the colon when ingested
and therein promote the growth of desirable (probiotic) Figure 1. Role of pre- and probiotics for skin care.
organisms. Examples include: fructooligosaccharides (FOS),
galactooligosaccharides, glucomannan oligosaccharides,
inulin, isomalto-oligosaccharides, lactosucrose, although this is not the case in other areas of the body, such
lactulose, neosugars, palatinose, raffinose, sorbitol, soy as the oral and vaginal cavities (Tester and Al-Ghazzewi,
oligosaccharides, xylitol and xylooligosaccharides (Al- 2013). Synbiotics have been claimed to have beneficial
Ghazzewi et al., 2007; Connolly et al., 2010; Roberfroid, effects in the treatment and prevention of gastrointestinal
2007; Tomasik and Tomasik, 2003; Van Loo et al., diseases (Ritchie and Romanuk, 2012). However, reports
1999). In cosmetic formulations, the term prebiotic can suggest the function extends beyond the gut by inducing
be applied ‘in principle’ to the skin microbiota where systemic effects on the skin (Ouwehand et al., 2002; Suzuki
the carbohydrates stimulate selectively the activity and et al., 2010). This has been discussed elsewhere in terms of
growth of beneficial ‘normal’ skin microbiota (Krutmann, the gut-associated lymphoid tissue system (Saavedra and
2009). Some carbohydrates, e.g. konjac glucomannan, Tschernia, 2002).
fructooligosaccharides, are capable of promoting skin health
in unique ways, especially the glucomannans (Al-Ghazzewi 2. Skin ecosystem
and Tester, 2010; Bateni et al., 2013).
Human skin is covered with a diverse multicellular
Synbiotics community of microorganisms (Grice and Segre, 2011).
These microbiota comprise bacteria and fungi in a
Both probiotics and prebiotics complement each other when diverse topography with typical counts of 10 2 to 107
used to improve health. A combination of the two concepts cells/cm2 reflecting their different niches (Findley et al.,
is called synbiotic (Fooks and Gibson, 2002; Gibson and 2013; Fredricks, 2001; Grice and Segre, 2011; Human
Roberfroid, 1995), where substrates can increase the Microbiome Project Consortium, 2012). Normal skin
survival of the probiotic strains. Su et al. (2007) found that microbiota are classified (Figure 2) as either ‘resident’ (i.e.
prebiotics enhance the survival and prolong the retention adhering predominantly to the skin, maintaining viability
period of specific probiotics by treating mice with soybean and reproducibility) or ‘transient’ (i.e. deposited but do
oligosaccharide (SOS), FOS or inulin, followed by probiotics not adhere to the surface of the skin, with little or no
Lactobacillus acidophilus LAFTI L10 (L10), Bifidobacterium sustained growth and reproduction) (Noble, 1981). The skin
lactis LAFTI B94 (B94) or Lactobacillus casei L26 LAFTI ecosystem is a complex environment due to the physical
(L26). Synbiotics have the capacity to optimise, maintain structure of the skin and the environmental factors it is
and restore the microbiota of the skin systemically or exposed to; hence (in the healthy state) it tends to resist
by topical applications (Figure 1). One major problem microbial colonisation (Bojar and Holland, 2002). In skin
with topical applications of probiotics, even in synbiotic care, exposure of the skin to rapidly changing external
formulations, is the harsh environmental conditions of the influences has a profound effect on the microbiological
skin, which prevent colonisation (Bojar and Holland, 2002), ecology. Influences from within the body, including diet

100 Beneficial Microbes 5(2)


 Impact of prebiotics and probiotics on skin health

(Propionibacterium acnes, Propionibacterium avidum


Yeast and Propionibacterium granulosum), coagulase-negative
Malassezia
furfur staphylococci (Staphylococcus epidermidis), micrococci,
corynebacteria, brevibacteria, Acinetobacter and the
yeast species Malassezia with some bacteriophages. Most
Gram +ve cocci Gram –ve bacilli
Micrococci (mostly): Acinetobacter common transient species are Staphylococcus aureus,
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M. luteus Streptococcus pyogenes, Escherichia coli and Pseudomonas


aeruginosa (Fredricks, 2001; Krutmann, 2009; Leyden et
al., 1987) as shown in Figure 2.
Gram +ve bacilli Gram +ve cocci
Propionibacterium (e.g. Staphylococci
P. acnes, P. avidium, (mostly): The number of microbial species on skin vary according
P. granulosum) S. epidermidis to the parts of the body and type of microflora (Kong
Corynebacterium S. haemolyticus
Brevibacterium S. hominis and Segre, 2012; Tester and Al-Ghazzewi, 2012). In
Dermatobacter
wet skin areas, aerobic bacteria counts range from 102
to 107 cells/cm2, while the anaerobic counts range from
Resident microbiota 104 to 106 cells/cm2 (Leyden et al., 1983; Noble, 1981).
Propionibacterium and Staphylococcus species are the most
Transient microbiota abundant in sebaceous sites, while Corynebacterium and
Staphylococcus species predominate in moist sites. In dry
sites, a mixed bacterial population seems to reside (Grice
Deposited on the skin
e.g. Staphylococcus aureus et al., 2008, 2009). Gao and colleagues (2010) quantified
Streptococcus pyogenes Propionibacterium, Corynebacterium, Streptococcus,
Pseudomonas aeruginosa
Bacillus Staphylococcus and Malassezia in six body locations
Escherichia coli (forehead, axillae, inner elbows, forearms, forelegs and
behind ears) of eight healthy subjects using real-time PCR.
The authors found that the highest counts of bacteria were
Figure 2. Normal skin microbiota composed of resident and in the axilla, while the forearm had the lowest counts.
transient microorganisms. Streptococcus was the most common bacterium on the
forehead and behind the ear, while Corynebacterium spp.
were predominant in the axilla. Malassezia spp. were
and hormones, have a considerable impact on the skin too found with only very low counts. Costello et al. (2009)
(Al-Ghazzewi and Tester, 2010). Stability is maintained reported that body sites across individuals, such as the
by interactions between different microbial species and palm and forearm, exhibited high microbial diversity,
between the host and microbiota. Microorganisms in this while other sights like the forehead showed less. This is
ecosystem are considered to be beneficial, some essentially due to the fact that the hands are the most frequent parts
neutral and some pathogenic (or have the capacity to be with which people touch various surfaces and various
pathogenic). Little has been done to optimise the favourable microorganisms persist on inanimate surfaces (Kramer et
ecology of the skin, which is a poorly understood area al., 2006). However, the forehead has a different ecology.
(Tester and Al-Ghazzewi, 2012). It is a lipid rich environment and thus may favour the
colonisation of P. acnes (convert triglycerides to free fatty
3. Skin microbiota acids), hence inhibiting other microorganisms, (Gribbon
et al., 1993; Shu et al., 2013; Thormar and Hilmarsson,
Exposure to hostile skin conditions on a frequent basis 2007) including S. aureus (Shu et al., 2013). Colonisation
means only a limited number of microbial types can of microbiota can also vary in association with progressive
colonise effectively. This actual colonisation varies sexual maturation. Oh et al. (2012) characterised and
between different parts of the body and is encouraged by compared the bacterial communities of four body sites
the presence of large amounts of water, proteins, lipids including skin parts for 28 healthy subjects aged 2 to 40
and where a little evaporation of water occurs (Leyden years. The authors found that Firmicutes (Streptococcaceae),
et al., 1987). All these factors are influenced by the Bacteroidetes and Proteobacteria were abundant in children,
environmental exposure of the body and bathing profiles, while Corynebacteriaceae and Propionibacteriaceae
and the constant association with clothes, age, genetic predominated in adults. For further details on the microbial
makeup and immune response play a role on colonisation community composition and diversity of skin microbiome
(Kong and Segre, 2012; Murillo and Raoult, 2013; Tester and its dynamics following skin barrier disruption, the
and Al-Ghazzewi, 2012). The types of microbes on the reader is referred to Zeeuwen et al. (2012).
skin include the resident species of propionibacteria

Beneficial Microbes 5(2) 101


F.H. Al-Ghazzewi and R.F. Tester

4. Pre- and probiotics for health a direct immunomodulatory effect on skin-associated


immune responses (Guéniche et al., 2008c). In addition,
Ingested probiotics (e.g. Lactobacillus bulgaricus, Guéniche and colleagues (2010a) have reported the effect
Lactobacillus plantarum, Lactobacillus casei) have of cream containing Bifidobacterium longum extract on
been shown to reduce acne symptoms by inhibiting the reactive skin. The authors found that subjects that applied
production of pro-inflammatory cytokines (Chiba et al., the cream had a significant decrease in skin sensitivity and
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2010; Chon et al., 2010; Paszti-Gere et al., 2012), which increase in skin resistance against physical and chemical
seem to act as mediators for the initiation of acne lesions aggression. Furthermore, the number of repeated tape
(Zouboulis et al., 2005). A number of studies have reported strippings (Gao et al., 2013) required to disrupt skin barrier
on the therapeutic effects of probiotics on atopic dermatitis function were increased in the treatment group. Thus,
(Betsi et al., 2008; Meneghin et al., 2012; Weston et al., some results support the hypothesis that probiotics might
2005; Yesilova et al., 2012). The assumption for efficacy is exert their beneficial effect beyond the gut and to the skin
that these beneficial effects occur systemically, by which (Bowe and Logan, 2011; Guéniche et al., 2009b, 2010b;
the probiotic microorganisms exert specific effects in the Philippe et al., 2011).
intestinal lumen and on epithelial cells and immune cells
with antiallergic potential (Caramia et al., 2008). Apparently, The enhancement of skin natural defences exerted by
the approach may induce a ‘glow of health’ as claimed by probiotics (Figure 3) occurs due to competition with
Levkovick et al. (2013). In a randomised double blind pathogens for nutrients, mucosal adherence, modulation
placebo-controlled clinical trial, Guéniche et al. (2009a) of mucosal immune functions and by production of
reported that certain probiotics, such as Lactobacillus antimicrobial metabolites like bacteriocins (O’Sullivan et al.,
johnsonii NCC 533 (La1), can modulate skin immune 2005; Santos et al., 2003; Todoriki et al., 2001; Van Reenen
systems leading to preservation of skin homeostasis et al., 1998; Verschuere et al., 2000). Not only do probiotics
(Guéniche et al., 2006a, 2008a; Peguet-Navarro et al., 2008). contribute towards this skin defence barrier, resident
bacteria can do so too. For example, S. epidermidis produces
Topical applications of probiotics have been reported antimicrobial peptides that can benefit cutaneous immune
(Farmer and Mikhail, 1998) to have a very direct effect defence systems (Cogen et al., 2008, 2010) by inhibiting
at the site of application, by inducing natural defence selectively S. aureus and Group A streptococci, while
mechanisms (Volz and Biedermann, 2009). A number maintaining normal skin microbiota (Cogen et al., 2010;
of studies have reported the beneficial effects of topical Gallo and Nakatsuji, 2011). The removal of skin resident
applications of Vitreoscilla filiformis on patients with species, for example S. epidermidis by topical antibiotics,
seborrhoeic dermatitis and atopic eczema (Guéniche et will eliminate endogenous antimicrobial peptides (Bastos
al., 2006b, 2008b). Although the specific mechanism of et al., 2009), allowing potentially pathogenic bacteria,
beneficial effects of the non-pathogenic Gram-negative such as S. aureus, to colonise the skin more effectively. As
bacterium on such diseases is not yet established, it may microbial diversity varies, another positive health effect
be due to a reduction of S. aureus counts and possibly of beneficial resident microbiota on skin is to fill niches

Prebiotics
Act as nutrient Non-preferential
sources nutrient use

(a) Bind to lectins


of pathogens
(b) Induce immune-support
Probiotics &
beneficial Growth = Inhibition
Pathogens
resident (a) Uses up the carbon source
bacteria (b) Produces acid and
(c) Other antimicrobial agents to
restrict/prevent pathogen growth
(d) Enhance immune functions

Reduce the capacity of Cause infections


infections to colonise skin Infections

Figure 3. Prebiotics stimulate the growth of probiotics and beneficial resident bacteria on skin and induce natural defence
mechanisms to inhibit the pathogens.

102 Beneficial Microbes 5(2)


 Impact of prebiotics and probiotics on skin health

that would otherwise be colonised by pathogens and indirect effect to prevent atopic diseases by suppressing
subsequently cause infection (Bojar and Holland, 2002; immunoglobulin E (IgE) production in mice and hence
Findley et al., 2013; Grice and Segre, 2011; Kong and prevent the development of dermatitis (Suzuki et al., 2010).
Segre, 2012). Propionibacteria may have beneficial effects, Although the exact mechanism of the effects of fermentable
such as adjuvant and anti-tumour activities. Hence these dietary fibres on the specific immune system in the gut has
attributes may contribute to more efficient immunological not yet been fully established, it has been suggested that
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responses to infections (Eady and Ingham, 1994). It should modulation of the intestinal microbiota occurs. This causes
be remembered, however, that the same species are of immune-enhancing effects by lactic acid bacteria in contact
pathogenic relevance in for example acne and folliculitis with immune cells in the intestine, the production of short
(Al-Ghazzewi and Tester, 2010). The pathogenicity of P. chain fatty acids (SCFAs) from the fibre degradation and/
acnes is probably due to a number of distinct phylogroups or by changes to the mucin production (Schley and Field,
with different phenotypes and virulences (Kwon et al., 2002). Glucomannans have also been reported to modulate
2013). These phylotype groups known as types IA1, IA2, skin bacterial proliferation and normalise sensitive skin
IB, IC, II and III may be associated with different types of barrier functionality (Berardesca et al., 2008). Onishi et al.
infections and clinical conditions (Nagy et al., 2013). Some (2007a) found that feeding pulverised konjac glucomannan
argue that the disease-causing potential of different P. acnes to mice suppressed the development of scratching
strains is not only determined by the phylotype-specific behaviour, substance ‘P’ expression with mastocytosis
genome content but also by variable gene expression and skin inflammatory immune responses. In addition,
(Brzuszkiewicz et al., 2011). administration of pulverised konjac glucomannan prevented
the development of allergic rhinitis-like symptoms and the
Prebiotics in general have been found to stimulate the increase of plasma IgE and immunoglobulin G levels in
immune system in vitro and in vivo (Swanson et al., 2002; mice (Onishi et al., 2003, 2005, 2007b; Oomizu et al., 2006).
Torrecillas et al., 2007; Yamada et al., 2003). They can
also stimulate the growth of probiotics at the expense of 5. Pre- and probiotics in commercial topical
pathogens, such as Salmonella typhimurium, Clostridium skin care products
perfringens, Listeria monocytogens, E. coli, S. aureus and
P. acnes (Al-Ghazzewi and Tester 2010; Al-Ghazzewi A number of products containing prebiotics, probiotics
et al., 2007, 2012, Elamir et al., 2008). Akiyama et al. or synbiotics are marketed commercially by the skin
(2002) reported that glucooligosaccharides can be used care industry. However, it seems that a limited range is
to control the growth of S. aureus, which often infects available for topical skin care products containing pre- or
or colonises patients with atopic dermatitis (Chase and probiotics at this time. These include mainly creams and
Armstrong, 2012). Al-Ghazzewi and Tester (2010) studied lotions formulated with either prebiotics, probiotics or
the synbiotic effects of konjac glucomannan hydrolysates both. Some of these products claim to protect hands and
on the growth of the skin bacterium P. acnes in vitro. The nails against bacteria. Others are designed for treating
authors concluded that the inhibition of the acne-induced dandruff, itching or rashes.
bacterium was significantly enhanced by the presence of
glucomannan hydrolysates. It is important to control the Prebiotics may or may not be soluble in skin care formats,
overgrowth of some resident bacteria, such as P. acnes which provide many challenges. Skin care products are
on skin, and prebiotics could be a candidate for this. In a alcohol- or oil-based and sometimes have a complex list
recent study by Bateni et al. (2013), it was found that topical of ingredients (Tester and Al-Ghazzewi, 2012). Often,
formulations of konjac glucomannan hydrolysates were skin products are designed to hide faults or to have a non-
able to exert a positive and direct impact on skin health, selective surface kill, e.g. alcohols and salicylic acid. The
reducing acne vulgaris in vivo and inducing a glow to skin. long term effects of this are not potentially conductive to
The authors suggested that there is a possible link between ‘good skin’. In addition, skin care products are designed to
the glucomannan hydrolysates and sebum gland physiology. provide colour, glow, healthiness, or to treat blemishes and
It is possible that the hydrolysates may contribute toward cuts and/or infections. There are considerable challenges to
unblocking the pores on skin surface and hence restore ensure that any desirable functionality required of the pre-
skin barrier properties and control superficial (and perhaps or probiotic is retained by contact with the skin. In many
within sebaceous glands) microbiota. situations this is hard to ensure due to the environmental
exposure of the body, hygiene and the constant association
Any effects of prebiotics in the gut can be reflected in/ with clothes. Positively, however, and unlike probiotics, any
on other parts of the body, such as the skin, vagina or potential efficacy of a prebiotic is retained in a formulation
bladder (Al-Ghazzewi and Tester, 2010; Sutherland et due to the relative stability of the carbohydrates (even in
al., 2008; Tester et al., 2012). Consuming prebiotics (e.g. relatively harsh formats). This can often not be the case for
hydrolysed konjac glucomannan) can have a positive but other types of skin intervention ingredients.

Beneficial Microbes 5(2) 103


F.H. Al-Ghazzewi and R.F. Tester

6. Overview Chase, E.P. and Armstrong, A.W., 2012. Advances in management


of atopic dermatitis: new therapies and novel uses of existing
The use of pre- and probiotics for skin care is in its infancy. treatments. Seminars in Cutaneous Medicine and Surgery 31: 17-24.
However, there are a number of products that are beginning Chiba, Y., Shida, K., Nagata, S., Wada, M., Bian, L., Wang, C., Shimizu,
to incorporate pre- and/or probiotics in their formulations. T., Yamashiro, Y., Kiyoshima-Shibata, J., Nanno, M. and Nomoto,
There are considerable challenges ahead but also many K., 2010. Well-controlled proinflammatory cytokine responses of
http://www.wageningenacademic.com/doi/pdf/10.3920/BM2013.0040 - Thursday, September 21, 2017 1:35:57 AM - Göteborgs Universitet IP Address:130.241.16.16

opportunities. Peyer’s patch cells to probiotic Lactobacillus casei. Immunology


130: 352-362.
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