Journal of Dermatological Science
Volume 54, Issue 1 , Pages 1-5, April 2009

Pre- and probiotics for human skin

Institut für Umweltmedizinische Forschung (IUF) at the Heinrich-Heine-University, Düsseldorf gGmbH, Auf’m Hennekamp 50, D-4025 Düsseldorf, Germany

Received 7 January 2009; accepted 20 January 2009. published online 12 July 2010.

Article Outline

Abstract 

Current research on the complex interplay between the microbiota, the barrier function and the innate immune system of the skin indicates that the skin's microbiota have a beneficial role, much like that of the gut microflora. As a consequence, interest in strategies beyond antibiotica that allow a more selective modulation of the skin microflora is constantly growing. This review will briefly summarize our current understanding of the cutaneous microbiota and summarize existing information on pre- and probiotic strategies for skin.

Keyword: Pre- and probiotics for human skin

 

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1. Introduction 

Prebiotics have been defined as “non-digestible food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one, or a limiting number of, bacteria in the colon” [1]. This concept has originally been developed for the gut, but in principle can be applied to modulate the composition of any microbial community including the skin microflora to achieve beneficial effects.

Scientific interest in the composition and function of the skin's microflora (=the skin's microbiota) is currently experiencing a revival, and in fact, has become one of the most exciting and rapidly developing areas in cutaneous biology [2]. A major driving force for this development has been the discovery that epidermal keratinocytes have the potential to affect the cutaneous microflora by producing antimicrobial peptides [3]. Also, recent research efforts to understand the control of skin barrier functions unambiguously point to a close link between physical, immunological and cell biological properties of the skin and its microflora [4], [5]. Manipulation of the composition and/or function of the skin microflora by prebiotic strategies, which, in contrast to antibiotics, may allow selective inhibition of detrimental and at the same time preservation and/or stimulation of beneficial bacteria, is therefore of obvious interest in dermatology [2].

In contrast to prebiotics, probiotics are based on the use of living organisms which upon ingestion in certain numbers exert health beneficial effects beyond inherent general nutrition [6]. Probiotics have been widely used for the treatment/prevention of gastrointestinal disorders, but a growing number of clinical studies suggest that probiotic strategies induce systemic effects which extend beyond the gut and may even affect selected functions of the skin [7]. Accordingly, modulation of the gut's microflora through probiotics appears to cause beneficial effects in healthy as well as diseased human skin [8], [9].

This article briefly summarizes the scientific basis for such strategies and provides a critical overview about the currently available studies on the use of pre- and/or probiotica in clinical dermatology and cosmetics.

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2. Microflora of human skin 

The normal human skin microflora is composed of a limited number of microbial types, as outlined below. This is a direct consequence of the unique environmental conditions the skin offers to microbes, which markedly differ from those found at mucosal surfaces. In other words only a limited number of microbial types (mainly Gram-positive species) have evolved to take advantage of the harsh environmental conditions that are being offered by the skin [10].

In general, resident and transient microbial species are present on the skin. The term resident refers to viable, reproducing populations, whereas transient species are defined as contaminants with little or no capacity for sustained growth and reproduction in the cutaneous environment. Resident microbial species include Proprionibacteria (P. acnes, P. avidum and P. granulosum), Coagulase-negative Staphylococci (Staphylococcus epidermidis), Micrococci, Corynebacteria and Acinetobacter. In addition, there are Malassezia yeast species and a variety of bacteriophage species. Common transient species are Staphylococcus aureus, Escherichia coli, Pseudomonas aeroguinosa and Bacillus species. It should be emphasized that the above said represents the “textbook” knowledge on the skin's microflora, which is limited to culture-dependent assays, although it is estimated that less than 1% of harvested species can be cultivated. More recent studies employing 16SrRNA gene survey strategies indicate that the human skin microbiota is far more complex [11], [12] and in fact comprises 113 phylotypes that belong to six bacterial divisions. Among these, Proteobacteria dominate the skin microbiota. In contrast, 16 SrRNA sequences that closely match S. epidermidis and P. acnes consisted of less than 6% of the captured microbiota. This is in clear contrast to the commonly held notion that S. epidermidis is the dominant aerobic bacteria resident in skin [11].

The resident microflora fills a niche that could otherwise be colonized by pathogenic microorganisms that are aggressive and cause infection, either at the skin site or by transfer to other sites. Also, if the skin could be colonized by pathogens adopted for other sites (e.g. mucous membranes), this could facilitate the spread of pathogens by offering them more dispersed routes.

This is, however, not the only positive function of the resident microflora. Accordingly, Propionibacteria have been shown to have adjuvant and antitumor activities and to contribute to a more efficient immunological response to general infections [13], [14]. On the other hand, the same species are of pathogenic relevance in acne and folliculitis [15]. In aggregate, preservation of the resident microflora is thought to be an effective way to achieve maintenance of healthy “normal” skin functions. It is only when the host becomes compromised by trauma, injury or changes in the immune defense that the resident microflora displays pathogenic potential. Under such circumstances, pathogenic effects not only are restricted to S. epidermidis, but may also be observed with Propionibacterium species. Thus, the resident microflora may be regarded as “beneficial” to the “normal, healthy” host, but may become dangerous to the host with disturbed skin integrity.

The limited number of microbial species that colonize human skin is determined by a variety of physical and biochemical factors [10], [16]. The physical factors are mainly defined by the host environment and include the number and size of follicles and glands, gland function, the flow of secretions, the integrity of barrier function, skin pH and osmotic potential. A slightly acidic pH, e.g., favors Proprionibacterium spp., whereas neutral and alkaline pH favors most other resident bacteria. Also, high hydration is associated with higher pH, which is again associated with high microbial population density, e.g., in the foot. Biochemical factors include chemical compounds such as soluble micronutrients derived from sebum (lipids and aminoacids) and sweat (vitamins, lactate and amino acids) as well as biochemical molecules which are produced as a consequence of the metabolic activity of microorganisms on the skin and which in turn function to influence colonization. Examples of microbial metabolites controlling other residents are lantibiotics produced by Staphylococcus spp. Other factors are methantiol, bacteriocins, organic acids and lytic enzymes, including those produced by bacteriophages. Also, bacterial metabolism affects pH and osmotic potential.

Another level of complexity is provided by the interplay between skin microorganisms and the skin immune system. The skin possesses the capacity to mount both, adaptive and non-adaptive immune responses. Non-adaptive (=innate) immune responses are immediate and non-specific, whereas adaptive immune responses are secondary and selective in nature.

There is currently no evidence to suggest that adaptive immune responses of the skin influence the normal skin microflora. There is, however, some evidence that the skin microflora activates the adaptive immune system. Accordingly, microorganisms on the skin have been shown to be coated with immunoglobulins which are most likely derived from eccrine gland secretions [17], [18]. Also, numerous reports have described humoral and cell-mediated immune responses in the peripheral blood against skin microbials (e.g., [19], [20], [21], [22], [23]). These studies did not clarify, however, whether stimulation of the adaptive immune system occurred via the skin or at a different site where the same or related species of microorganisms reside. In favor of first possibility is the observation that in pityriaisis versicolor, seborrheic dermatitis and dandruff, the immune response to Malassezia species is maintained at higher levels as compared to healthy control subjects [14], [24]. Similar observations have also been made in acne patients for immune response against P. acnes [25].

In marked contrast to adaptive immune responses, non-adaptive, innate immune responses of the skin are clearly involved in the control of microbial colonization. Accordingly, upon activation by microorganisms, epidermal keratinocytes have the capacity to produce all four known β-defensins as well as cathelicidin hCAP-18 and by producing these antimicrobial peptides inhibit growth or kill microorganisms, i.e. bacteria and also viruses.

A detailed review of the relative importance of these factors and their complex interplay can be found in Ref. [26]. In the context of this review it is important to state that skin microflora, skin barrier function and the skin immune system are closely linked to each other and appear to form a complex and highly regulated network that controls a variety of fundamental skin functions. It is therefore no surprise that attempts have been made beyond antibiotica to selectively manipulate this system in order to achieve beneficial effects for human skin.

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3. Prebiotics and skin 

As outlined above the composition of the skin microflora depends on numerous factors and thus the bacterial equilibrium can easily be disturbed. A prominent example is skin of acne patients where overgrowth of P. acnes has been observed [15]. Conventional cosmetic strategies to correct this problem not only make use of antibacterial agents which are effective in reducing the amount of P. acnes, but at the same time also affect other, beneficial bacteria such as S. epidermidis, which is regarded as a commensal bacterium that serves to protect human skin from infections and other environmental insults, as outlined before. In this regard, a prebiotic strategy that would rebalance the composition of the skin's microflora by inhibiting the growth of P. acnes and at the same time preserving the growth of beneficial bacteria seems preferable (Fig. 1). Accordingly, recent studies demonstrate the successful development of a prebiotic cosmetic approach to balance the composition of the cutaneous microflora. In these studies skin microflora was analyzed by fluorescence in situ hybridization [27]. This very precise method avoids the drawbacks of cultural methods and allows the direct observation of bacteria on the skin [28]. It was observed that twice daily application of a cosmetic product containing selected plant extracts from either Ginseng or Black currant or pine to human skin for a total of three weeks was effective in inhibiting the growth of P. acnes, whereas coagulase negative staphylococci were not affected [27]. This study thus demonstrates that it is generally feasible to improve the composition of the skin microflora, i.e. to limit or reduce the growth of pathogenic species and at the same time to preserve or even stimulate the growth of beneficial bacteria. In this regard, such a prebiotic cosmetic approach is clearly superior to antibacterial cosmetic products which unselectively reduce bacterial growth by means of antibiotics or antimicrobial agents [29]. It should be kept in mind, however, that the design of this study was open and the number of volunteers was limited to 11. Further studies are therefore clearly needed to confirm these preliminary observations.

It will also be of interest to access whether and how colonization of human skin with “beneficial” bacteria such as S. epidermidis causes beneficial effects in human skin that extend beyond the prevention of overgrowth of human skin by pathogenic bacteria. Theoretically, the presence of S. epidermidis could affect the skin barrier function and/or the development of innate immune responses in human skin. Such a bidirectional relationship between the skin and its microflora would provide the basis for the development of prebiotic strategies for the treatment of skin diseases with known deficiencies in barrier function and innate immunity such as atopic eczema [30].

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4. Probiotics and skin 

In contrast to the very limited number of studies on the use of prebiotic strategies in cosmetic and dermatology, a constantly growing body of the literature exists about the relevance of probiotics for skin. It is now generally believed that probiotics exert beneficial effects by improving the characteristics of the intestinal microflora. Most studies have used lactic acid bacteria, i.e. lactobacilli, enterococci and bifidobacteria, that are able to survive through the stomach and small intestine [7]. Probiotic lactic acid bacteria have been linked to many effects including improving rates of recovery from gastroenteritis and diarrhoea of viral and bacterial origins [31], [32], [33], [34]. They have been suggested to modulate immunity in the gut but also systemically, and the latter property may be of relevance for human skin [35]. Accordingly, a significant improvement on the course of atopic dermatitis has been reported in infants given probiotic-supplemented elimination diets [36], [37], [38], [39]. Also, probiotics administered pre- and postnatally for 6 months may be able to reduce the prevalence of atopic eczema in children at high risk for atopic diseases as compared with placebo treatment [8], although this preventive effect of probiotics is controversial [40]. The mechanistic basis of skin effects induced by probiotic gut flora is thought to be represented by changes in systemic immune responses. In particular, modulation of specific T-cell subsets such as stimulation of TH1 cells in the gut mucosa which may subsequently influence immune responses in other tissues may play a role [41], [42], [43]. Also, in mice, oral administration of Lactobacillus casei reduced contact hypersensitivity to a hapten only in the presence of CD4+ T-cells, which control the size of the CD8+ effector pool [44].

It has been speculated that not only diseased, but also healthy skin may profit from the oral ingestion of probiotic bacteria (Fig. 2). Accordingly, nutritional supplementation of hairless mice with Lactobacillus johnsonii provided protection of the skin immune system against ultraviolet B radiation-induced immunosuppressive effects [45]. Similar effects have recently been described in a human in vivo study and it has been proposed that oral consumption of probiotic bacteria may represent a novel approach to protect the skin immune system against ultraviolet radiation [46]. Another target for probiotics may be skin barrier function. A recent double-blind, randomized clinical study has shown that a 24-week skin nutrition intervention with a fermented dairy product in female volunteers having dry and sensitive, but otherwise healthy skin significantly reduced transepidermal water loss and thus improved stratum corneum barrier function compared to a placebo product [47]. It should be noted, however, that in addition to the probiotic strains (L. casei, Lactobacillus bulgaris and Stretococcus thermophilus) this dairy product contained a mixture of boretsch oil, green tea polyphenols and vitamin E and that skin barrier improvement may be at least in part due to these ingredients.

  • View full-size image.
  • Fig. 2. 

    Oral ingestion of probiotics exerts beneficial effects on the skin through mechanisms which are presumably initiated in the gut. Alternatively, after topical application, probiotics may directly act on skin.

All these approaches have been based on the oral application of probiotic strains. There is, however, at least circumstantial evidence that beneficial effects can also be achieved by topical application of probiotic bacteria to human skin (Fig. 2). In general, nonintestinal applications of probiotics are few and have thus far mainly been used for the urogenital tract There are currently only a very few studies pursuing a probiotic approach for the skin microflora. In this regard [48], point out the difficulty to identify useful bacteria in view of the harsh environmental conditions that may prevent colonization of skin with a probiotic strain. Nevertheless, results from two studies suggest that topical application of Vitreoscilla filiformis exerts beneficial effects in patients with seborrheic dermatitis and atopic eczema [49], [50]. V. filiformis is a Gram-negative bacteria found in thermal spa water from LaRoche-Posay, France, and classically used for dermatological treatment. Although the precise mechanisms through which V. filiformis improves skin symptoms in atopic and seborrheic dermatitis are not yet known it is tempting to speculate that immunomodulatory effects are at least partially involved. This assumption is supported by very recent studies indicating that V. filiformis has profound effects on the skin immune system (T. Biedermann, personal communication).

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Acknowledgements 

This work has been supported by the Deutsche Forschungsgemeinschaft SFB 728 and GRK 1033.

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biography

Jean Krutmann is a professor of Dermatology and Environmental Medicine at the Heinrich-Heine-University, Düsseldorf, Germany. He holds appointments as an adjunct professor at CWRU and UAB, USA as well as Nagoya City University, Japan. He is the Director of IUF, an Institute of the Scientific Community Leibniz (WGL). He has received numerous scientific awards including C.E.R.I.E.S, has published more than 200 original papers and several monographs. He currently serves on the board of directors of the International Union of Photobiology, the European and the American Society of Photodermatology.

PII: S0923-1811(09)00024-3

doi:10.1016/j.jdermsci.2009.01.002

Journal of Dermatological Science
Volume 54, Issue 1 , Pages 1-5, April 2009

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