THE JOURNAL OF ALTERNATIVE AND COMPLEMENTARY MEDICINE Volume 21, Number 7, 2015, pp. 380–385 ª Mary Ann Liebert, Inc. DOI: 10.1089/acm.2014.0261
Review Article
Effects of Fermented Dairy Products on Skin: A Systematic Review Alexandra R. Vaughn, BS,1 and Raja K. Sivamani, MD, MS, CAT 2
Abstract
Objective: Fermented dairy products, such as yogurt, have been proposed as a natural source of probiotics to promote intestinal health. Growing evidence shows that modulation of the gastrointestinal tract microbiota can modulate skin disease as well. This systematic review was conducted to examine the evidence for the use of ingested fermented dairy products to modulate skin health and function. We also sought to review the effects of the topical application of dairy products. Design: The PubMed and Embase databases were systematically searched for clinical studies involving humans only that examined the relationship between fermented dairy products and skin health. Results: A total of 312 articles were found and a total of 4 studies met inclusion criteria. Three studies evaluated the effects of ingestion, while one evaluated the effects of topical application. All studies noted improvement with the use of fermented dairy. Conclusions: Overall, there is early and limited evidence that fermented dairy products, used both topically and orally, may provide benefits for skin health. However, existing studies are limited and further studies will be important to better assess efficacy and the mechanisms involved.
Introduction
T
he skin acts as the primary barrier between the internal and external environments. It provides critical protection against microorganisms and chemical, mechanical, and sun damage. Nutritional supplementation is becoming more widely used, and there is great interest to adapt this to dermatology for a variety of skin conditions. Diet plays a key role in medicine, and current nutritional science continues to find deeper understanding of the prominent influence of food intake on skin health.1 More physicians and patients are utilizing nutritional supplementation as alternative or complementary therapy to standard drug treatments for various skin conditions.2 Specific food ingredients may demonstrate to be biologically active in modulating skin function and appearance. For instance, it is known that in cases of nutritional deficiencies, supplementation with the deficient minerals, vitamins, and fatty acids improves those skin conditions.3 Dairy products come in many different forms and may influence skin health. Dairy products provide important nutrients, including vitamin A, vitamin B12, niacin, and zinc.4 However, dairy has also been reported to exacerbate some skin conditions, such as acne.5 The fermentation of 1 2
dairy converts lactose to lactic acid and has several known health benefits. Lactic acid has been used topically for decades to rejuvenate sun-damaged skin and reduce hyperpigmentation, with concentrations ranging from mild creams to in-office chemical peels. Proposed mechanisms for these effects of topically applied lactic acid may include promoting exfoliation through loss of intercellular adhesion6 and by modulating the cytokine milieu surrounding the keratinocytes.7 In the digestive system, it promotes digestibility8 and gastrointestinal (GI) tract health by maintaining the microbiota that are essential to digestive function. These GI microbiota provide a protective barrier for the host and may prevent disease of the gut.9 For example, modulating the microbiota environment of the intestines may change inflammation-related colon cancer susceptibility.10 However, there is growing evidence that modulating the inflammatory state of the GI tract can modulate the skin as well.11 It is unclear how lactic acid may benefit inflammatory skin diseases, including acne and eczema, and whether ingested fermented dairy is superior to topically applied products. The evidence showing how fermented foods regulate the lining of the GI system poses the question of how fermented dairy could influence the skin in similar ways.
Drexel University College of Medicine, Philadelphia, PA. Department of Dermatology, University of California–Davis, Sacramento, CA.
380
FERMENTED DAIRY PRODUCTS ON SKIN
381
Fermented dairy products, also known as cultured dairy products, are dairy foods containing lactic acid-producing bacteria such as Lactobacillus and Bifidobacterium.12 Fermented dairy products have been suggested to provide antiinflammatory and antimicrobial benefits in inflammatory skin conditions such as atopic dermatitis.13 The objective of this review is to evaluate the existing evidence regarding how fermented dairy products influence skin health. We systematically review clinical studies examining the effects of fermented dairy products, both applied topically and ingested, on the skin.
Results
Materials and Methods
Topically applied fermented products
On July 29, 2014, we systematically searched PubMed and Embase for published clinical studies examining the use of fermented dairy products to improve skin health. The PubMed database was searched using the MeSH terms ‘‘yogurt,’’ ‘‘cultured milk products,’’ ‘‘lactobacillus,’’ ‘‘dermatology,’’ ‘‘skin,’’ and ‘‘skin diseases.’’ We also included other terms that fall under the ‘‘cultured milk product,’’ category, including ‘‘labneh,’’ ‘‘dahi,’’ ‘‘lassi,’’ ‘‘clabber,’’ ‘‘amasi,’’ ‘‘kefir,’’ ‘‘chal,’’ ‘‘curd,’’ ‘‘filmjolk,’’ ‘‘kumia,’’ ‘‘smetena,’’ and ‘‘viili.’’ Embase database was searched using Emtree search terms ‘‘yogurt,’’ ‘‘cultured milk products,’’ ‘‘dermatology,’’ ‘‘skin,’’ and ‘‘skin diseases,’’ along with the same family of cultured milk products as above, ‘‘labneh,’’ ‘‘dahi,’’ ‘‘lassi,’’ ‘‘clabber,’’ ‘‘amasi,’’ ‘‘kefir,’’ ‘‘chal,’’ ‘‘curd,’’ ‘‘filmjolk,’’ ‘‘kumia,’’ ‘‘smetena,’’ and ‘‘viili.’’ Both searches were filtered to only include clinical studies involving humans and those written in English. Bibliographies were searched for additional studies that met inclusion and exclusion criteria. Both of the authors independently evaluated the results for inclusion in the systematic review. Of 312 articles found, 4 articles met inclusion criteria (see Fig. 1).
One study examined the efficacy of topically applied yogurt in improving elasticity, water content, and melanin.14 This study concluded that using yogurt supplied ample moisture and helped to maintain the barrier and retain elasticity of the skin. They did not find any changes in melanin although the length of exposure to the yogurt was not described. The dermal irritation studies were performed over 24 hours and this exposure time would not be sufficient to ascertain changes in melanin. Previous work by others15,16 has demonstrated that lactic acid may increase skin thickness and promote epidermal remodeling, thereby improving the skin barrier, which may explain in part the results of this study using topically applied yogurt. A study by Yamamoto et al.17 demonstrates that topically applied lactic acid at an optimal pH promotes epidermal thickening and dermal procollagen 1 production, while a much lower pH leads to more severe epidermal changes and possible tissue damage.
FIG. 1.
Search strategy and results.
The studies that met inclusion criteria are summarized in Table 1. Fermented milk products were studied as both topical and oral therapies for skin health. One study examined the effects of topically applied yogurt, while the others evaluated orally ingested fermented products. Two studies evaluated changes in the skin’s properties such as elasticity and its barrier function. Two studies evaluated the effects on atopy and atopic dermatitis, while another evaluated the effects on acne.
Orally ingested fermented products
One study revealed that lactoferrin-enriched fermented milk improves symptoms of acne vulgaris compared to supplementing with lactoferrin alone.18 Lactoferrin is known to have antimicrobial and anti-inflammatory action by sequestering iron that is essential for bacterial growth.19 However, this study demonstrated that ingestion of both fermented milk and lactoferrin decreased the symptoms of acne. In another study, skin barrier function was examined after ingesting fermented milk with borage oil.20 Borage oil contains the anti-inflammatory omega-6 fatty-acid, gamma linolenic acid (GLA). GLA has been shown to be highly important for skin function.21 Skin barrier function, as measured by transepidermal water loss, was significantly improved in the group with borage oil and fermented milk as opposed to the group with borage oil and nonfermented milk. Another study reported significant improvements that ingested yogurt has on subjective symptoms and intestinal environment in patients with atopic dermatitis.22 Compared to the control group, the yogurt group had a significant improvement in itching and burning sensations. Additionally, intestinal metabolites, including the polyamine spermidine (SMD) and the short-chain fatty acid butyrate, were significantly increased in the yogurt group. Increased SMD due to the yogurt consumption improved the intestinal barrier in the atopic dermatitis patients. Increased butyrate offers better maintenance of intestinal epithelial cells.
382
Fermented dairy product
Lactobacillus casei–, L. bulgaricus–, and S. thermophilus– fermented milk with borage oil, green tea, and vitamin E
Puch et al.20 Ingested
6-mo, open, double-blind, randomized clinical study
4-wk, doubleblind, placebocontrolled, crossover study
12-wk, open, double-blind, randomized clinical study
Ingested
Ingested
Randomized controlled trial
Study design
Topical
Topical or ingested dairy
SCFA, short chain fatty acids; TEWL, transepidermal water loss.
Bifidobacterium animalis subsp. lactis LKM512 yogurt
Matsumoto et al.22
Yeom et al.14 Topically applied yogurt containing Lactobacillus bulgaricus and Streptococcus thermophilus Kim et al.18 Lactoferrin-enriched fermented milk (using L. bulgaricus and S. thermophilus)
Study
72
10
Intractable atopic dermatitis
1. Acne lesion counts & Significant improvement in acne vulgaris in the lactoferrin grades group only 2. Hydration, sebum, pH, and skin surface Decreased sebum production in both the lactoferrin-enriched lipids milk and the placebo group (fermented milk) 1. Subjective symptoms 1. Improvement in itch and burning in 4/10 & 3/8 patients (itch, burn, pain, taking LKM512 irritation, visual 2. Significant increase in status) polyamine SMD in LKM512 2. Intestinal microbiota groups 3. Intestinal bacterial 3. Significant increase in SCFA metabolites butyrate in 8/10 of LKM512 (polyamines, SCFA) group 4. Th1/Th2 balance Barrier function, Skin barrier function measured as TEWL significantly improved in fermented milk group vs. nonfermented milk group
Significantly improved moisture and maintenance of elasticity in yogurt group vs. control group
Major results
56
Major outcome measures Moisture, TEWL, melanin, elasticity, subjective symptoms
Acne vulgaris
Disease assessed
16
Number of subjects
Table 1. Summary of Clinical Studies
FERMENTED DAIRY PRODUCTS ON SKIN
Table 2. Fermented Dairy Products of the World Fermented dairy product Labneh Dahi Lassi Clabber Amasi Kefir Chal Curd Filmjolk Kumia Smetana Viili
Country of origin Middle East India and Pakistan Bangladesh, India, and Pakistan Ulster Scots of Ireland South Africa Eastern and Northern Europe Central Asia Worldwide Nordic Countries Central Asia Central and Eastern Europe Nordic Countries
Together, these metabolites lead to a much healthier intestinal environment, which is proposed to lead to a better balance of Th1-type cells versus Th-2-type cells. Discussion Market for naturally based ingredients
An increasing number of patients are asking for naturally based extracts and ingredients as supplementary dermatologic remedies.23 Patients are increasingly looking beyond
383
their prescription medications and procedures for more natural and cost-effective treatments to improve their skin.24 According to the Global Cosmeceuticals Market Outlook 2018 Report, the market for the use of botanicals, naturals products, and cosmeceuticals for dermatology was estimated to be $35 billion and is the fastest growing market of the personal care industry.25 Therefore, it is of importance for dermatologists to be informed about the evidence for the use of natural ingredients, such as yogurt. Fermented products
Fermented dairy products can be found all over the world (Table 2). Fermented milk contains Lactobacillus acidophilus; typical commercial yogurt contains the bacterial strains Streptococcus thermophilus and Lactobacillus bulgaricus, and sometimes also L. acidophilus and Bifidobacterium; and kefir contains L. acidophilus, Lactobacillus casei, and Lactobacillus reuteri.26 As seen above, there is some variation in the bacterial strains in various forms of fermented dairy products. Possible mechanisms
Evidence suggests that fermented dairy products promote a healthy GI environment, which may allow for benefits, including improved lactose intolerance, protection against GI infections, and relief of constipation.27 Based on the
FIG. 2. Schematic of how lactic acid-rich fermented dairy products may be beneficial to the gut epithelium and reduce systemic inflammation. GI, gastrointestinal.
384
beneficial effects that fermented foods have on promoting a healthy GI system, several mechanisms have been proposed for how they may interact with the skin. The gut microbiota may influence systemic and skin inflammation.28 For example, small intestine bacterial overgrowth (SIBO) has been associated with rosacea and scleroderma.11,29 Treatments that reduce SIBO have been shown to improve rosacea.30 Exposure to probiotics has been shown to reduce SIBO,31 although studies directly evaluating the influence of probiotics on acne and rosacea are still needed.32 It remains unclear how the gut and the skin may communicate, but some studies suggest that there may be circulating endotoxins that may influence skin inflammation.33 Furthermore, fermentation and probiotics may enhance the intestinal mucosal barrier, regulate the immune system, inhibit pathogens, help carry out essential enzymatic reactions, and produce important metabolites for the host34 (see Fig. 2). As research in this field grows, more of the mechanistic connections between the gut and the skin will be uncovered. It is still not clear whether oral or topical fermented dairy would be more beneficial for skin-related outcomes. Ingested fermented dairy products may provide unique benefits in modulating the gut microbiota, while topical fermented dairy may more directly modulate the skin microflora and directly modulate inflammation. Comparative studies are needed to better understand the differences between topical and oral use. To ascertain changes in skin appearance, studies will need to be conducted over a time frame such that the changes can be ascertained. For example, one study evaluated melanin production and concluded that there was no change in melanin.14 However, this study only evaluated subjects over 24 hours and a much longer evaluation period, over a period of 2–3 months, would be needed to accurately ascertain changes in melanin. Limitations
Interpretation of our search results is limited by the few number of studies found, small sample sizes, methodology of study design, and fermentation characteristic variations. The reproducibility of similar studies should consider the fermentation preparation, including identical bacterial strains and fermentation loads. Conclusions
There is some clinical evidence that fermented dairy products, used both topically and orally, may provide benefits to overall skin health and the treatment of some skin diseases. Dermatologists should be aware of the clinical studies that continue to test the use of fermented dairy products as alternative or complementary skin care therapies. Many different cultures in different parts of the world use fermented dairy products as diet staples. If these fermented products prove to provide clinically significant benefits to skin health, dermatologists may consider incorporating this natural remedy to improve skin diseases and overall skin health and beauty. Our search of the PubMed and Embase databases yielded a very low number of search results for how fermented dairy products may improve skin health. Therefore, more methodically controlled clinical studies are needed to assess how fermentation products could be used topically and orally to improve various skin conditions.
VAUGHN AND SIVAMANI Acknowledgment
We thank Bruce Abbott for his assistance in conducting the systematic search algorithms. Author Disclosure Statement
No competing financial interests exist. References
1. Piccardi N, Manissier P. Nutrition and nutritional supplementation: Impact on skin health and beauty. Dermatoendocrinology 2009;1:271–274. 2. Dickinson A, Shao A, Boyon N, Franco JC. Use of dietary supplements by cardiologists, dermatologists and orthopedists: Report of a survey. Nutr J 2011;10:20. 3. Boelsma E, van de Vijver LP, Goldbohm RA, et al. Human skin condition and its associations with nutrient concentrations in serum and diet. Am J Clin Nutr 2003;77:348– 355. 4. Basavaraj KH, Seemanthini C, Rashmi R. Diet in dermatology: Present perspectives. Indian J Dermatol 2010; 55:205–210. 5. Melnik BC. Evidence for acne-promoting effects of milk and other insulinotropic dairy products. Nestle Nutrition workshop series. Paediatr Programme 2011;67:131–145. 6. Wang X. A theory for the mechanism of action of the alpha-hydroxy acids applied to the skin. Med Hypotheses 1999;53:380–382. 7. Rendl M, Mayer C, Weninger W, Tschachler E. Topically applied lactic acid increases spontaneous secretion of vascular endothelial growth factor by human reconstructed epidermis. Br J Dermatol 2001;145:3–9. 8. Martini MC, Lerebours EC, Lin WJ, et al. Strains and species of lactic acid bacteria in fermented milks (yogurts): Effect on in vivo lactose digestion. Am J Clin Nutr 1991; 54:1041–1046. 9. Macfarlane GT, Macfarlane S. Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int 2012;95:50–60. 10. Uronis JM, Muhlbauer M, Herfarth HH, et al. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PloS One 2009;4:e6026. 11. Parodi A, Paolino S, Greco A, et al. Small intestinal bacterial overgrowth in rosacea: Clinical effectiveness of its eradication. Clin Gastroenterol Hepatol 2008;6:759–764. 12. Shiby VK, Mishra HN. Fermented milks and milk products as functional foods—a review. Crit Rev Food Sci Nutr 2013;53:482–496. 13. Betsi GI, Papadavid E, Falagas ME. Probiotics for the treatment or prevention of atopic dermatitis: A review of the evidence from randomized controlled trials. Am J Clin Dermatol 2008;9:93–103. 14. Yeom G, Yun DM, Kang YW, et al. Clinical efficacy of facial masks containing yoghurt and opuntia humifusa raf. (F-YOP). J Cosmet Sci 2011;62:505–514. 15. Bernstein EF, Underhill CB, Lakkakorpi J, et al. Citric acid increases viable epidermal thickness and glycosaminoglycan content of sun-damaged skin. Dermatol Surg 1997;23: 689–694. 16. Usuki A, Ohashi A, Sato H, et al. The inhibitory effect of glycolic acid and lactic acid on melanin synthesis in melanoma cells. Exp Dermatol 2003;12 Suppl 2:43–50. 17. Yamamoto Y, Uede K, Yonei N, et al. Effects of alphahydroxy acids on the human skin of Japanese subjects: The rationale for chemical peeling. J Dermatol 2006;33:16–22.
FERMENTED DAIRY PRODUCTS ON SKIN
18. Kim J, Ko Y, Park YK, et al. Dietary effect of lactoferrinenriched fermented milk on skin surface lipid and clinical improvement of acne vulgaris. Nutrition 2010;26:902–909. 19. Ling JM, Schryvers AB. Perspectives on interactions between lactoferrin and bacteria. Biochem Cell Biol 2006; 84:275–281. 20. Puch F, Samson-Villeger S, Guyonnet D, et al. Consumption of functional fermented milk containing borage oil, green tea and vitamin E enhances skin barrier function. Exp Dermatol 2008;17:668–674. 21. Ziboh VA, Cho Y, Mani I, Xi S. Biological significance of essential fatty acids/prostanoids/lipoxygenase-derived monohydroxy fatty acids in the skin. Arch Pharm Res 2002;25: 747–758. 22. Matsumoto M, Aranami A, Ishige A, et al. LKM512 yogurt consumption improves the intestinal environment and induces the T-helper type 1 cytokine in adult patients with intractable atopic dermatitis. Clin Exp Allergy 2007;37:358–370. 23. Reuter J, Merfort I, Schempp CM. Botanicals in dermatology: An evidence-based review. Am J Clin Dermatol 2010;11:247–267. 24. Levin J, Momin SB. How much do we really know about our favorite cosmeceutical ingredients? J Clin Aesth Dermatol 2010;3:22–41. 25. Global Cosmeceuticals Market Outlook 2018. 2014. Available at http://www.sbdi.co.kr/cart/data/info/RNCOS_ Global_Cosmeceuticals_Market_Outlook_2018_sample.pdf? ckattempt =1, accessed March 2015. 26. Heller KJ. Probiotic bacteria in fermented foods: Product characteristics and starter organisms. Am J Clin Nutr 2001;73:374s–379s. 27. Buttriss J. Nutritional properties of fermented milk products. Int J Dairy Technol 1997;50:21–27.
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28. Bowe WP, Logan AC. Acne vulgaris, probiotics and the gut-brain-skin axis—Back to the future? Gut Pathogens 2011;3:1. 29. Parodi A, Sessarego M, Greco A, et al. Small intestinal bacterial overgrowth in patients suffering from scleroderma: Clinical effectiveness of its eradication. Am J Gastroenterol 2008;103:1257–1262. 30. Weinstock LB, Steinhoff M. Rosacea and small intestinal bacterial overgrowth: Prevalence and response to rifaximin. J Am Acad Dermatol 2013;68:875–876. 31. Barrett JS, Canale KE, Gearry RB, et al. Probiotic effects on intestinal fermentation patterns in patients with irritable bowel syndrome. World J Gastroenterol 2008;14:5020– 5024. 32. Bowe WP. Probiotics in acne and rosacea. Cutis 2013;92: 6–7. 33. Bowe W, Patel NB, Logan AC. Acne vulgaris, probiotics and the gut-brain-skin axis: From anecdote to translational medicine. Beneficial Microbes 2014;5:185–199. 34. Ceapa C, Wopereis H, Rezaiki L, et al. Influence of fermented milk products, prebiotics and probiotics on microbiota composition and health. Best practice & research. Clin Gastroenterol 2013;27:139–155.
Address correspondence to: Raja K. Sivamani, MD, MS, CAT Department of Dermatology University of California–Davis 3301 C Street, Suite 1400 Sacramento, CA 95816 E-mail: [email protected]
Review Article
Effects of Fermented Dairy Products on Skin: A Systematic Review Alexandra R. Vaughn, BS,1 and Raja K. Sivamani, MD, MS, CAT 2
Abstract
Objective: Fermented dairy products, such as yogurt, have been proposed as a natural source of probiotics to promote intestinal health. Growing evidence shows that modulation of the gastrointestinal tract microbiota can modulate skin disease as well. This systematic review was conducted to examine the evidence for the use of ingested fermented dairy products to modulate skin health and function. We also sought to review the effects of the topical application of dairy products. Design: The PubMed and Embase databases were systematically searched for clinical studies involving humans only that examined the relationship between fermented dairy products and skin health. Results: A total of 312 articles were found and a total of 4 studies met inclusion criteria. Three studies evaluated the effects of ingestion, while one evaluated the effects of topical application. All studies noted improvement with the use of fermented dairy. Conclusions: Overall, there is early and limited evidence that fermented dairy products, used both topically and orally, may provide benefits for skin health. However, existing studies are limited and further studies will be important to better assess efficacy and the mechanisms involved.
Introduction
T
he skin acts as the primary barrier between the internal and external environments. It provides critical protection against microorganisms and chemical, mechanical, and sun damage. Nutritional supplementation is becoming more widely used, and there is great interest to adapt this to dermatology for a variety of skin conditions. Diet plays a key role in medicine, and current nutritional science continues to find deeper understanding of the prominent influence of food intake on skin health.1 More physicians and patients are utilizing nutritional supplementation as alternative or complementary therapy to standard drug treatments for various skin conditions.2 Specific food ingredients may demonstrate to be biologically active in modulating skin function and appearance. For instance, it is known that in cases of nutritional deficiencies, supplementation with the deficient minerals, vitamins, and fatty acids improves those skin conditions.3 Dairy products come in many different forms and may influence skin health. Dairy products provide important nutrients, including vitamin A, vitamin B12, niacin, and zinc.4 However, dairy has also been reported to exacerbate some skin conditions, such as acne.5 The fermentation of 1 2
dairy converts lactose to lactic acid and has several known health benefits. Lactic acid has been used topically for decades to rejuvenate sun-damaged skin and reduce hyperpigmentation, with concentrations ranging from mild creams to in-office chemical peels. Proposed mechanisms for these effects of topically applied lactic acid may include promoting exfoliation through loss of intercellular adhesion6 and by modulating the cytokine milieu surrounding the keratinocytes.7 In the digestive system, it promotes digestibility8 and gastrointestinal (GI) tract health by maintaining the microbiota that are essential to digestive function. These GI microbiota provide a protective barrier for the host and may prevent disease of the gut.9 For example, modulating the microbiota environment of the intestines may change inflammation-related colon cancer susceptibility.10 However, there is growing evidence that modulating the inflammatory state of the GI tract can modulate the skin as well.11 It is unclear how lactic acid may benefit inflammatory skin diseases, including acne and eczema, and whether ingested fermented dairy is superior to topically applied products. The evidence showing how fermented foods regulate the lining of the GI system poses the question of how fermented dairy could influence the skin in similar ways.
Drexel University College of Medicine, Philadelphia, PA. Department of Dermatology, University of California–Davis, Sacramento, CA.
380
FERMENTED DAIRY PRODUCTS ON SKIN
381
Fermented dairy products, also known as cultured dairy products, are dairy foods containing lactic acid-producing bacteria such as Lactobacillus and Bifidobacterium.12 Fermented dairy products have been suggested to provide antiinflammatory and antimicrobial benefits in inflammatory skin conditions such as atopic dermatitis.13 The objective of this review is to evaluate the existing evidence regarding how fermented dairy products influence skin health. We systematically review clinical studies examining the effects of fermented dairy products, both applied topically and ingested, on the skin.
Results
Materials and Methods
Topically applied fermented products
On July 29, 2014, we systematically searched PubMed and Embase for published clinical studies examining the use of fermented dairy products to improve skin health. The PubMed database was searched using the MeSH terms ‘‘yogurt,’’ ‘‘cultured milk products,’’ ‘‘lactobacillus,’’ ‘‘dermatology,’’ ‘‘skin,’’ and ‘‘skin diseases.’’ We also included other terms that fall under the ‘‘cultured milk product,’’ category, including ‘‘labneh,’’ ‘‘dahi,’’ ‘‘lassi,’’ ‘‘clabber,’’ ‘‘amasi,’’ ‘‘kefir,’’ ‘‘chal,’’ ‘‘curd,’’ ‘‘filmjolk,’’ ‘‘kumia,’’ ‘‘smetena,’’ and ‘‘viili.’’ Embase database was searched using Emtree search terms ‘‘yogurt,’’ ‘‘cultured milk products,’’ ‘‘dermatology,’’ ‘‘skin,’’ and ‘‘skin diseases,’’ along with the same family of cultured milk products as above, ‘‘labneh,’’ ‘‘dahi,’’ ‘‘lassi,’’ ‘‘clabber,’’ ‘‘amasi,’’ ‘‘kefir,’’ ‘‘chal,’’ ‘‘curd,’’ ‘‘filmjolk,’’ ‘‘kumia,’’ ‘‘smetena,’’ and ‘‘viili.’’ Both searches were filtered to only include clinical studies involving humans and those written in English. Bibliographies were searched for additional studies that met inclusion and exclusion criteria. Both of the authors independently evaluated the results for inclusion in the systematic review. Of 312 articles found, 4 articles met inclusion criteria (see Fig. 1).
One study examined the efficacy of topically applied yogurt in improving elasticity, water content, and melanin.14 This study concluded that using yogurt supplied ample moisture and helped to maintain the barrier and retain elasticity of the skin. They did not find any changes in melanin although the length of exposure to the yogurt was not described. The dermal irritation studies were performed over 24 hours and this exposure time would not be sufficient to ascertain changes in melanin. Previous work by others15,16 has demonstrated that lactic acid may increase skin thickness and promote epidermal remodeling, thereby improving the skin barrier, which may explain in part the results of this study using topically applied yogurt. A study by Yamamoto et al.17 demonstrates that topically applied lactic acid at an optimal pH promotes epidermal thickening and dermal procollagen 1 production, while a much lower pH leads to more severe epidermal changes and possible tissue damage.
FIG. 1.
Search strategy and results.
The studies that met inclusion criteria are summarized in Table 1. Fermented milk products were studied as both topical and oral therapies for skin health. One study examined the effects of topically applied yogurt, while the others evaluated orally ingested fermented products. Two studies evaluated changes in the skin’s properties such as elasticity and its barrier function. Two studies evaluated the effects on atopy and atopic dermatitis, while another evaluated the effects on acne.
Orally ingested fermented products
One study revealed that lactoferrin-enriched fermented milk improves symptoms of acne vulgaris compared to supplementing with lactoferrin alone.18 Lactoferrin is known to have antimicrobial and anti-inflammatory action by sequestering iron that is essential for bacterial growth.19 However, this study demonstrated that ingestion of both fermented milk and lactoferrin decreased the symptoms of acne. In another study, skin barrier function was examined after ingesting fermented milk with borage oil.20 Borage oil contains the anti-inflammatory omega-6 fatty-acid, gamma linolenic acid (GLA). GLA has been shown to be highly important for skin function.21 Skin barrier function, as measured by transepidermal water loss, was significantly improved in the group with borage oil and fermented milk as opposed to the group with borage oil and nonfermented milk. Another study reported significant improvements that ingested yogurt has on subjective symptoms and intestinal environment in patients with atopic dermatitis.22 Compared to the control group, the yogurt group had a significant improvement in itching and burning sensations. Additionally, intestinal metabolites, including the polyamine spermidine (SMD) and the short-chain fatty acid butyrate, were significantly increased in the yogurt group. Increased SMD due to the yogurt consumption improved the intestinal barrier in the atopic dermatitis patients. Increased butyrate offers better maintenance of intestinal epithelial cells.
382
Fermented dairy product
Lactobacillus casei–, L. bulgaricus–, and S. thermophilus– fermented milk with borage oil, green tea, and vitamin E
Puch et al.20 Ingested
6-mo, open, double-blind, randomized clinical study
4-wk, doubleblind, placebocontrolled, crossover study
12-wk, open, double-blind, randomized clinical study
Ingested
Ingested
Randomized controlled trial
Study design
Topical
Topical or ingested dairy
SCFA, short chain fatty acids; TEWL, transepidermal water loss.
Bifidobacterium animalis subsp. lactis LKM512 yogurt
Matsumoto et al.22
Yeom et al.14 Topically applied yogurt containing Lactobacillus bulgaricus and Streptococcus thermophilus Kim et al.18 Lactoferrin-enriched fermented milk (using L. bulgaricus and S. thermophilus)
Study
72
10
Intractable atopic dermatitis
1. Acne lesion counts & Significant improvement in acne vulgaris in the lactoferrin grades group only 2. Hydration, sebum, pH, and skin surface Decreased sebum production in both the lactoferrin-enriched lipids milk and the placebo group (fermented milk) 1. Subjective symptoms 1. Improvement in itch and burning in 4/10 & 3/8 patients (itch, burn, pain, taking LKM512 irritation, visual 2. Significant increase in status) polyamine SMD in LKM512 2. Intestinal microbiota groups 3. Intestinal bacterial 3. Significant increase in SCFA metabolites butyrate in 8/10 of LKM512 (polyamines, SCFA) group 4. Th1/Th2 balance Barrier function, Skin barrier function measured as TEWL significantly improved in fermented milk group vs. nonfermented milk group
Significantly improved moisture and maintenance of elasticity in yogurt group vs. control group
Major results
56
Major outcome measures Moisture, TEWL, melanin, elasticity, subjective symptoms
Acne vulgaris
Disease assessed
16
Number of subjects
Table 1. Summary of Clinical Studies
FERMENTED DAIRY PRODUCTS ON SKIN
Table 2. Fermented Dairy Products of the World Fermented dairy product Labneh Dahi Lassi Clabber Amasi Kefir Chal Curd Filmjolk Kumia Smetana Viili
Country of origin Middle East India and Pakistan Bangladesh, India, and Pakistan Ulster Scots of Ireland South Africa Eastern and Northern Europe Central Asia Worldwide Nordic Countries Central Asia Central and Eastern Europe Nordic Countries
Together, these metabolites lead to a much healthier intestinal environment, which is proposed to lead to a better balance of Th1-type cells versus Th-2-type cells. Discussion Market for naturally based ingredients
An increasing number of patients are asking for naturally based extracts and ingredients as supplementary dermatologic remedies.23 Patients are increasingly looking beyond
383
their prescription medications and procedures for more natural and cost-effective treatments to improve their skin.24 According to the Global Cosmeceuticals Market Outlook 2018 Report, the market for the use of botanicals, naturals products, and cosmeceuticals for dermatology was estimated to be $35 billion and is the fastest growing market of the personal care industry.25 Therefore, it is of importance for dermatologists to be informed about the evidence for the use of natural ingredients, such as yogurt. Fermented products
Fermented dairy products can be found all over the world (Table 2). Fermented milk contains Lactobacillus acidophilus; typical commercial yogurt contains the bacterial strains Streptococcus thermophilus and Lactobacillus bulgaricus, and sometimes also L. acidophilus and Bifidobacterium; and kefir contains L. acidophilus, Lactobacillus casei, and Lactobacillus reuteri.26 As seen above, there is some variation in the bacterial strains in various forms of fermented dairy products. Possible mechanisms
Evidence suggests that fermented dairy products promote a healthy GI environment, which may allow for benefits, including improved lactose intolerance, protection against GI infections, and relief of constipation.27 Based on the
FIG. 2. Schematic of how lactic acid-rich fermented dairy products may be beneficial to the gut epithelium and reduce systemic inflammation. GI, gastrointestinal.
384
beneficial effects that fermented foods have on promoting a healthy GI system, several mechanisms have been proposed for how they may interact with the skin. The gut microbiota may influence systemic and skin inflammation.28 For example, small intestine bacterial overgrowth (SIBO) has been associated with rosacea and scleroderma.11,29 Treatments that reduce SIBO have been shown to improve rosacea.30 Exposure to probiotics has been shown to reduce SIBO,31 although studies directly evaluating the influence of probiotics on acne and rosacea are still needed.32 It remains unclear how the gut and the skin may communicate, but some studies suggest that there may be circulating endotoxins that may influence skin inflammation.33 Furthermore, fermentation and probiotics may enhance the intestinal mucosal barrier, regulate the immune system, inhibit pathogens, help carry out essential enzymatic reactions, and produce important metabolites for the host34 (see Fig. 2). As research in this field grows, more of the mechanistic connections between the gut and the skin will be uncovered. It is still not clear whether oral or topical fermented dairy would be more beneficial for skin-related outcomes. Ingested fermented dairy products may provide unique benefits in modulating the gut microbiota, while topical fermented dairy may more directly modulate the skin microflora and directly modulate inflammation. Comparative studies are needed to better understand the differences between topical and oral use. To ascertain changes in skin appearance, studies will need to be conducted over a time frame such that the changes can be ascertained. For example, one study evaluated melanin production and concluded that there was no change in melanin.14 However, this study only evaluated subjects over 24 hours and a much longer evaluation period, over a period of 2–3 months, would be needed to accurately ascertain changes in melanin. Limitations
Interpretation of our search results is limited by the few number of studies found, small sample sizes, methodology of study design, and fermentation characteristic variations. The reproducibility of similar studies should consider the fermentation preparation, including identical bacterial strains and fermentation loads. Conclusions
There is some clinical evidence that fermented dairy products, used both topically and orally, may provide benefits to overall skin health and the treatment of some skin diseases. Dermatologists should be aware of the clinical studies that continue to test the use of fermented dairy products as alternative or complementary skin care therapies. Many different cultures in different parts of the world use fermented dairy products as diet staples. If these fermented products prove to provide clinically significant benefits to skin health, dermatologists may consider incorporating this natural remedy to improve skin diseases and overall skin health and beauty. Our search of the PubMed and Embase databases yielded a very low number of search results for how fermented dairy products may improve skin health. Therefore, more methodically controlled clinical studies are needed to assess how fermentation products could be used topically and orally to improve various skin conditions.
VAUGHN AND SIVAMANI Acknowledgment
We thank Bruce Abbott for his assistance in conducting the systematic search algorithms. Author Disclosure Statement
No competing financial interests exist. References
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Address correspondence to: Raja K. Sivamani, MD, MS, CAT Department of Dermatology University of California–Davis 3301 C Street, Suite 1400 Sacramento, CA 95816 E-mail: [email protected]
