The microbiome and aging
1Department of Dermatology, Miguel Servet University Hospital, IIS Aragón, Zaragoza 50009, Spain.
2Department of Dermatology, San Jorge General Hospital, Huesca 22004, Spain.
Correspondence to: Dr. Isabel Abadías-Granado, Department of Dermatology, Miguel Servet University Hospital, Paseo Isabel la Católica, 1-3, Zaragoza 50009, Spain. E-mail:
The microbiota changes as the host ages, but also the relationship between host and bacteria impacts host aging and life expectancy. Differences in the composition of certain bacterial species in the human gut and skin microbiome have been identified between the elderly and the young. In this sense, it has been suggested that the manipulation of the microbiota of older adults would be an innovative strategy in the prevention and treatment of age-related comorbidities.
Humans are practically sterile during gestation, but, as early as birth, the whole body surface, including the oral cavity, gut, and skin, are colonized by an enormous variety of microbes, fungal, archaeal, bacterial, and viral. There is a very complex relationship between the resident microbial communities and the human cells. These species and their metabolic products play an important role in a wide range of biological functions. In normal life, these microbes are necessary for many functions, such as developing and maintaining our immune system or digesting food. However, the dysfunction of the human microbiota is considering a relevant factor in many diseases[1,3].
The skin, the largest organ of the human body, is in direct and continuous contact with the external environment, and, consequently, it is exposed to the microorganisms that inhabit it. In addition, these skin commensal microbial communities interact with each other, as well as with the host cells and the immune system. In this sense, it is clear that the immunological system of the host modulates the composition of these communities, and, conversely, the microbes present on the skin have a great impact on human immune system[3,5].
Different factors influence the diversity in the composition of this ecosystem. In fact, the anatomy and physiology of the skin determine the skin bacterial diversity, such as the axillae, forehead, palms, fingers, or feet. Even on a particular niche of the body, the skin microbiota is still complicated by a combination of both external and internal factors, including, but not limited to, gender, age, environmental conditions such as pollution and the climate, genetics, hormones, cosmetics, diet, immune response, and lifestyles in general[5-8].
In this regard, different distributions of microorganism species have been identified in sebaceous, moist, or dry locations[6,8,9]. In addition, areas more exposed to the outside environment may contain a greater proportion of “transitory” microorganisms, compared to less exposed ones[6,9].
The perception of the skin as an ecosystem can help us to understand the delicate balance between host and microorganisms and how the alteration of any of them can result in skin diseases or infections.
The objective of this article is to review the existing evidence in relation to the microbiome and aging, especially that of the skin, and the possibility of manipulating the microbiome to prevent and treat age-related comorbidities and premature skin aging.
This is a narrative review of the subject. We obtained the articles by searching in PubMed. The search terms were microbiome, aging, skin, and skin cancer. To identify the articles relevant to the purposes of the review, we read abstracts, results, and, when necessary, the full texts to ascertain which ones contain pertinent information.
THE TECHNIQUES FOR SKIN MICROBIAL ANALYSIS
There are two main sampling methods for collecting resident skin microbiota. On the one hand, skin swabbing using a sterile cotton swab is a simple, quick, and non-invasive method for large-scale skin sampling. However, this method can accurately collect only resident microbiota from the stratum corneum; therefore, it does not provide a full spectrum picture of the skin microbiota, particularly in some specific subniches, such as the dermis. On the other hand, punch biopsies are invasive but offer the best representation of skin microbiota in deep epidermis, dermis, and glands such as the sebaceous gland. Nevertheless, due to its invasive nature, the latter is rarely used for qualitative analyses.
Regarding the technique, it must be sterile to ensure that bacterial DNA sequences are not introduced into the sample from sampling equipment, lab reagents, clinicians, etc.. Additionally, cold storage at -20 or
Once the samples are obtained and properly stored, there are several methods to extract DNA, including the REPLI-g Midi kit (Qiagen, Limberg, The Netherlands), Qiagen DNA Extraction Kit (Qiagen), and DNeasy DNA Extraction kit (Qiagen). These techniques recognize the specific DNA or RNA (16S ribosomal RNA) fingerprint sequences that each organism contains, which allows identifying, characterizing, and measuring the true relative abundance of each bacterial operational taxonomic units.
Finally, the essential portion of accurate microbiome analysis is the bioinformatics processing. Generally, large-scale computing clusters and specific bioinformatic pipelines must be established to understand and analyze these diverse bacterial communities from the millions of sequencing reads.
THE MICROBIOME OF THE SKIN
The majority of the “regular” bacterial inhabitants of the skin are included in four phyla: Actinobacteria, Proteobacteria, Bacteroidetes, and Firmicutes. The three most common genera are Propionibacteria, Corynebacteria, and Staphylococci.
The commensal microbes of the skin have also been classified as resident or transient depending on if they belong to the fixed microbiota or not[3,10]. The fixed microbiota tends to reestablish after disturbance. It is considered as commensal, which means that these microorganisms are normally harmless and most likely provide some benefit to the host. Transient microorganisms are temporarily found in the skin. They come from the environment and persist for hours or days and then disappear. Under normal circumstances, both groups are nonpathogenic. Recent research has shown that, even though the skin is constantly exposed to the environment, the healthy human skin microbiome is stable[12,13].
The body site is one of the most influential factors in the types of microbes inhabiting the skin. The three main types of environments on the human skin are sebaceous, dry, and moist. Moist areas mostly include the body folds: the navel, axilla, antecubital and popliteal fossa, or groin. Sebaceous areas include the forehead, nasolabial folds, retroauricular crease, middle chest, and back, whereas the upper buttock area, forearm, and hypothenar palm are drier sites[3,6,8-10]. Other microenvironments include the hair follicles, sweat glands, and dermal layers.
The microbial communities found in these cutaneous environments are different. Corynebacterium and Staphylococcus genera, of the phyla Actinobacteria and Firmicutes, respectively, are the most abundant microbes colonizing moist regions. The diversity of the microbes present in sebaceous sites is lower. In this anaerobic lipid-rich environment, there is a higher density of Propionibacterium, a lipophilic genus. The dry areas of the skin show the highest diversity in microbial inhabitants, predominantly Staphylococcus, Propionibacterium, Micrococcus, Corynebacterium, Enhydrobacter, and Streptococcus species[3,10]. Addition-ally, even microenvironments such as sebaceous, apocrine, and eccrine glands and hair follicles are associated with their own singular microbiota. In this sense, whereas Propionibacterium is especially adapted to the anaerobic environment rich in lipids of the sebaceous follicles, Gram-positive bacteria of the genera Corynebacterium, Micrococcus, Staphylococcus, and Propionibacterium are the main microbiota of the axillar area, rich in sebaceous glands.
Although microbiota research has focused primarily on identifying bacteria, we have to keep in mind that other types of microorganisms also live on the skin[3,10]. The fungal community is similar all over the body regardless of physiology. The genus Malassezia predominates at the head, trunk, and upper extremities, whereas feet are colonized by a combination of Malassezia, Aspergillus, Epicoccum, Rhodotorula, Cryptococcus, and other genera. Demodex is a tiny mite that is also present in normal skin, especially inside the follicles, although its role as a commensal organism remains uncertain. To our knowledge, there is little information about the viral composition of the cutaneous microbiota.
All these communities of bacteria, viruses, fungi, and mites present in different skin ecosystems can influence the health of the host in both senses, either as a protective mechanism disease or by contributing to the initiation or development of different dermatoses and cutaneous infections[11,15].
Regarding the biological mechanisms that could explain the relationship between the alteration in the skin microbiota and the development of disease, its role inducing inflammation and modulation of the immune response is considered very important[16-18]. All these microorganisms can produce beneficial or pathogenic substances, and the interaction among them can also participate in the pathophysiology of some dermatoses. Examples of dysbiosis related to skin diseases include: increase density of pathogenic bacteria, such as in atopic dermatitis; reduced bacterial diversity, such as in psoriasis; increase of commensal organisms, such as in acne; and alterations of microenvironments and colonization by unique species, such as in chronic wounds [Table 1].
Dysbiosis related to skin diseases
|Atopic dermatitis||Psoriasis||Acne vulgaris||Chronic wounds||AK/cutaneous SCC|
|90% of AD patients are colonized with Staphylococcus aureus on both lesional and non-lesional skin (compared with less than 5% of healthy individuals)
There is an increase in anaerobic bacterial species, including Clostridium and Serratia
|Higher levels of Proteobacteria on the trunk
Higher levels of Streptococcus and Propionibacterium in lesions
|Different Propionibacterium acnes strains between acne patients and healthy controls||Proliferation of several different anaerobic bacteria, including Staphylococcus, Serratia and Clostridium||Higher relative abundance of Propionibacterium and Malassezia on nonlesional skin than in AK/SCC lesions
S. aureus overabundance in AK/SCC
|Increased microbial load at the lesion site||Less microbial diversity in psoriatic lesions||Similar relative abundance of P. acnes between both groups but colonization of the affected follicles by multiple bacterial species in addition to P. acnes, including other commensal microorganisms, such as Streptococcus epidermidis||Decreased bacterial diversity
Opportunistic colonization of specifically adapted microbes
|More studies are required to expand and confirm these findings|
THE MICROBIOME AND AGING
The microbiota changes as the host ages, but also it seems that the relationship between the host and the microbiota impacts host aging and life expectancy. The changes in the microbiota with age have been extensively studied in the human gut. In this sense, there is a proliferation of opportunistic Proteobacteria at the cost of symbionts Firmicutes and Bacteroidetes with age, as well as less abundance of Bifidobacterium
Dysbiosis in aging
|Gut||Decrease of Bifidobacterium||Unchanged or decrease
Not seem to be related to the ageing
|Changes in the proportion: decrease in Clostridium and increase in Bacilli||Enrichment in facultative anaerobes, notably “pathobionts” (opportunistic components that can induce pathology, such as Enterobacteriaceae)|
|Actinobacteria is not highly represented in the human gut||Bacteroidetes and Firmicutes dominate the gut microbiota (93%-95%)||There is a proliferation of opportunistic Proteobacteria at the cost of symbionts Firmicutes and Bacteroidetes|
|Skin||Lower abundance in the older group, in relation to the decrease in the Propionibacterium genus. However, Corynebacterium significantly increase in the elderly||Increase||Increase; however, Staphylococcus genus is significantly decreased in the older group||Increase, especially the Acinetobacter genus|
|Actinobacteria is the predominant phyla in the skin|
|Oral||Increase in Actinomyces||Increase in Lactobacillales and Staphylococcus||Increase in Enterobacteriaceae and Pseudomonas|
|Oral bacteria contribute to bacterial diversification and alteration in the older skin: Streptococcus and Veillonella (F), Rothia (A), Prevotella (B), Haemophilus (P), and Fusobacterium are members of the core taxa of the oral bacterial community that are significantly enriched in the older skin microbiome.|
THE MICROBIOME AND SKIN AGING
The skin structure and function change with age, and this could be due not only to intrinsic factors such as cellular metabolisms, the immune system, or hormone changes, but also to extrinsic factors such as ultraviolet irradiation. In this sense, the microbiota also changes over the lifetime, not only due to age, but also due to geography, age, diet, lifestyle, and pollution, among others[8,25-27] [Figure 1].
Skin aging is characterized by a decrease in sebum and hydration levels as well as immune dysfunction, which results in significant alterations in skin physiology. These physiological changes also imply changes in the cutaneous ecology, inducing a disbalance of cutaneous microbiota.
The composition of the microbiome is different in old and young skin[7,30,31]. In puberty, the density of lipophilic bacteria proportionally increases with the increase of sebum levels, whereas it is much lower in elderly skin[5,32]. Moreover, metagenomic studies have shown a decrease of Actinobacteria in older skin[32,33]. However, the number of total bacteria increases in older people; specifically, more Corynebacterium species are found on the aged skin. Shibagaki et al. found that the diversification of skin microbiome in older skin is related to chronological and physiological skin aging, but it is related to the oral bacteria composition. Another study suggests that gut, oral, and skin microbiomes predict chronological age, being the skin microbiome the most accurate to predict it, on average yielding predictions within 4 years of chronological age [Table 1].
Nevertheless, some authors consider that changes in skin microbiota are also a consequence of aging, rather than a cause.
As research on the skin microbiome progresses, there is growing interest in finding ways to help the skin to recover and regenerate from the numerous microorganisms living on it. In this sense, the manipulation of the gut microbiota of older adults could be an innovative strategy in the prevention and treatment of age-related comorbidities; therefore, a balanced skin microbiota could help to prevent premature skin aging. Recently, oral and topical probiotics have been proposed as a therapy for restoration of the microbiota balance, supporting skin barrier function, as well as protecting against environmental factors, especially ultraviolet radiation-induced skin damage[36-38]. The following are some examples of relevant effects in the skin caused by different microorganism: Streptococcus thermophiles enhance ceramide levels of the stratum corneum when is topically applied on the skin; and some probiotics help to restore the balance between free radical removal and production, which may slow aging. On the other hand, oral and topical compounds are being investigated to know their potential therapeutic effect on the modulation of the skin microbiome: Orobanche rapum extract stimulates skin rejuvenation and protects the cutaneous microbiota, inducing healthier skin. In addition, the term “Photobiomics” has recently been introduced, referring to the use of low levels of visible or near-infrared light to modify the gut microbiome through photobiomodulation.
THE MICROBIOME AND SKIN CANCER
The occurrence of malignancies increases with age. The association between the microbiome and malignancies is a recent and not very well studied hypothesis also in skin cancer. Different studies suggest the role of microbiome in the tumoral genesis and/or progression, especially the gastrointestinal one. Additionally, the gut microbiota seems to play an important role in the response to immunotherapy, and, perhaps, this could also be extrapolated to the skin microbiota[16,17].
Some of this work indicates that dysbiosis may promote cancer. In normal circumstances, the microbiome does not induce a pro-inflammatory response due to the tolerance that the immune system has developed to commensal bacteria, preserving homeostasis. When these mechanisms are disrupted or new pathogenic microorganisms enter into this balanced system, dysbiosis occurs and the immune system is activated towards the microbiome, causing inflammation[18,44] or modifying the local immune response, which can trigger the tumoral growth in the intestine[16,17]. It has also been reported that intestinal inflammation enhances the possibility of the microbiota to produce genotoxins that cause damage to DNA, promoting the development of tumors.
Focusing on skin cancer, Mrázek et al. conducted a study on pigs, showing that the bacterial diversity was significantly different between normal skin and melanoma surface. They found that Trueperella and Fusobacterium genera were present in the microbiome of melanoma samples, which also had an increased amount of Streptococcus and Staphylococcus compared to the microbiome of normal skin. Moreover, Fusobacterium nucleatum increased with age in animals with progressive melanoma, whereas it diminished when animals had regressive disease. The authors concluded that Fusobacteria might be associated with tumor progression, and, as a possible mechanism, they proposed a tumor-based immune evasion: F. nucleatum - bound tumors are protected against the immune system, inhibiting natural killer cell cytotoxicity through the interaction of the fusobacterial protein Fap2 with the inhibitory receptor TIGIT of the immune cells. F. nucleatum can bind to different tumor types, including melanoma.
Recent studies suggest that some microorganisms of the skin microbiome can suppress tumor growth. In this sense, dysbiosis would be potentially harmful because the host microbiota loses its protective function and/or gains a harmful microbial community. This study describes a strain of Staphylococcus epidermidis common in the microbiota of the skin that produces 6-N-hydroxyaminopurine (6-HAP), a molecule that inhibits DNA polymerase activity. In culture, 6-HAP selectively inhibited the proliferation of tumor cell lines but did not inhibit normal keratinocytes. Intravenous injection of 6-HAP in mice suppressed melanoma growth without evidence of systemic toxicity. Colonization of mice with a strain of S. epidermidis producing 6-HAP reduced the chronic ultraviolet radiation skin damage and developing of tumors compared to mice colonized by a control strain that did not produce 6-HAP. S. epidermidis strains producing 6-HAP have been found in the metagenome from the skin of multiple healthy human subjects, suggesting that the microbiome of some individuals may protect against skin cancer. These findings show a new role for skin commensal bacteria in host defense against skin cancer induced by ultraviolet radiation.
Wang et al. proposed an in vitro model irradiating with co-cultures of human melanocytes and commensal skin bacteria containing Propionibacterium acnes and S. epidermidis. Commensal S. epidermidis and its byproduct lipoteic acid (LPA or TLR2 ligand, which has specific anti-inflammatory action on keratinocytes, increasing UVB resistance) promote melanocyte survival after UVB irradiation; this effect is due to an upregulation of TRAF1, CASP5, CASP14, and TP73; however, P. acnes induces apoptosis of UVB-irradiated melanocytes mediated by TNF-alpha production. The apparently opposite effects can be explained by the different location and concentration of P. acnes in the normal skin. P. acnes is found primarily in hair follicles, whose environment is critical for the maintenance of stem cells. Considering that DNA damage in these cells can result in severe mutations, P. acnes may have been accepted during evolution in the hair follicle niche to contribute to the health of the stem cell niche. By contrast, S. epidermidis is more present in dry areas of the body, especially on the inter-follicular epidermis. As mentioned above, LTA helps melanocytes to escape from UVB-induced apoptosis, which is crucial to preserve viable inter-follicular melanocytes during sun exposure, preventing their transformation into tumoral cells. Other studies that support this perspective include previous observations from the intestinal microbiome probing that microbes may suppress tumor growth by the production of short-chain free fatty acids[49,50]. Additionally, skin microbiota potentially produce cis-urocanic acid by degrading L-histidine, which plays a role in the immunosuppression induced by UV radiation and suppresses melanoma growth.
To our knowledge, there are few human studies investigating the relationship between the skin microbiome and skin cancer. One of them did not find significant differences in the diversity or abundance of bacterial genera between the microbiome of cutaneous melanomas and melanocytic nevi, although the cohort was relatively small (17 nevi and 15 melanoma).
Regarding non-melanoma skin cancer, a recent study investigated the microbiomes of actinic keratosis (AK) and cutaneous squamous cell carcinoma (SCC) in immunocompetent men either longitudinally or cross-sectionally. Propionibacterium and Malassezia were relatively most frequently found in healthy perilesional areas, whereas Staphylococcus was more abundant in both AK and SCC, with a predominance of the S. aureus species. Particularly, eleven Operational Taxonomic Units (OTUs) of S. aureus were identified in the participating subjects; six of these were significantly associated with SCCs, with OTUs 50 and 216 present in all patients, suggesting their specific involvement in progression from AK to SCC. Lately, these results have been confirmed, finding an overabundance of S. aureus in SCC and AK compared with basal cell carcinoma samples. Consequently, as Malassezia was decreased in SCCs, it is hypothesized that this yeast could be protective against S. aureus over-colonization [Table 1].
According to this local possible pathogenic effect of the skin microbiota in the promotion and/or progression of skin cancer, a recent study established the role of the gut microbiota in the response to anti-PD-1 immunotherapy in patients with metastatic melanoma. A significant association between the presence of some specific bacteria such as Bifidobacterium longum, Collinsella aerofaciens, and Enterococcus faecium and a positive clinical response to the therapy was found. According to this, reconstitution of germ-free mice with fecal material from responders improved tumor control, enhanced T cell responses, and increased efficacy of anti-PD-L1 therapy. These results suggest that commensal microbiome may modulate anti-tumor immunity in cancer patients.
Multiple studies indicate that age plays a critical role in modifying the human microbiota.
Furthermore, it appears that the microbiota may interact with ultraviolet radiation, facilitating skin damage and skin cancer or protecting against them. This knowledge opens the possibility of modulating the microbiota to maintain or improve health during aging. Thus, topical and oral probiotics are a promising therapy in the prevention of premature skin aging.
Conceptualization, investigation, writing original draft: Abadías-Granado I
Investigation, writing original draft: Sánchez-Bernal J
Conceptualization, supervision, writing, review and editing: Gilaberte YAvailability of data and materials
Not applicable.Financial support and sponsorship
None.Conflicts of interest
All authors declared that there are no conflicts of interest.Ethical approval and consent to participate
Not applicable.Consent for publication
© The Author(s) 2021.
1. Morgan XC, Huttenhower C. Chapter 12: Human microbiome analysis. PLoS Comput Biol 2012;8:e1002808.
2. Szabó K, Erdei L, Bolla BS, Tax G, Bíró T, Kemény L. Factors shaping the composition of the cutaneous microbiota. Br J Dermatol 2017;176:344-51.
3. Sanford JA, Gallo RL. Functions of the skin microbiota in health and disease. Semin Immunol 2013;25:370-7.
4. Rosenthal M, Goldberg D, Aiello A, Larson E, Foxman B. Skin microbiota: microbial community structure and its potential association with health and disease. Infect Genet Evol 2011;11:839-48.
6. Grice EA, Kong HH, Conlan S, et al. Topographical and temporal diversity of the human skin microbiome. Science 2009;324:1190-2.
7. Wilantho A, Deekaew P, Srisuttiyakorn C, Tongsima S, Somboonna N. Diversity of bacterial communities on the facial skin of different age-group Thai males. PeerJ 2017;5:e4084.
8. Ying S, Zeng DN, Chi L, et al. The influence of age and gender on skin-associated microbial communities in urban and rural human populations. PLoS One 2015;10:e0141842.
9. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA. The application of ecological theory toward an understanding of the human microbiome. Science 2012;336:1255-62.
10. Dréno B, Araviiskaia E, Berardesca E, et al. Microbiome in healthy skin, update for dermatologists. J Eur Acad Dermatol Venereol 2016;30:2038-47.
11. Weyrich LS, Dixit S, Farrer AG, Cooper AJ, Cooper AJ. The skin microbiome: Associations between altered microbial communities and disease. Australas J Dermatol 2015;56:268-74.
12. Oh J, Byrd AL, Park M, Kong HH, Segre JA. NISC Comparative Sequencing Program. Temporal stability of the human skin microbiome. Cell 2016;165:854-66.
14. Lacey N, Ní Raghallaigh S, Powell FC. Demodex mites--commensals, parasites or mutualistic organisms? Dermatology 2011;222:128-30.
15. Stecher B, Hardt WD. The role of microbiota in infectious disease. Trends Microbiol 2008;16:107-14.
16. Yu Y, Champer J, Beynet D, Kim J, Friedman AJ. The role of the cutaneous microbiome in skin cancer: lessons learned from the gut. J Drugs Dermatol 2015;14:461-5.
17. Russo E, Taddei A, Ringressi MN, Ricci F, Amedei A. The interplay between the microbiome and the adaptive immune response in cancer development. Therap Adv Gastroenterol 2016;9:594-605.
18. Wu S, Rhee KJ, Albesiano E, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 2009;15:1016-22.
21. Biagi E, Nylund L, Candela M, et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 2010;5:e10667.
22. Claesson MJ, Jeffery IB, Conde S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 2012;488:178-84.
23. Smith P, Willemsen D, Popkes M, et al. Regulation of life span by the gut microbiota in the short-lived African turquoise killifish. Elife 2017;6:e27014.
24. Bonté F, Girard D, Archambault JC, Desmoulière A. Skin changes during ageing. Subcell Biochem 2019;91:249-80.
25. Wu L, Zeng T, Deligios M, et al. Age-related variation of bacterial and fungal communities in different body habitats across the young, elderly, and centenarians in Sardinia. mSphere 2020;5:e00558-19.
26. Zapata HJ, Quagliarello VJ. The microbiota and microbiome in aging: potential implications in health and age-related diseases. J Am Geriatr Soc 2015;63:776-81.
27. Leung MHY, Tong X, Bastien P, et al. Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants. Microbiome 2020;8:100.
28. Russell-Goldman E, Murphy GF. The pathobiology of skin aging: new insights into an old dilemma. Am J Pathol 2020;190:1356-69.
29. Prescott SL, Larcombe DL, Logan AC, et al. The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming. World Allergy Organ J 2017;10:29.
30. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science 2009;326:1694-7.
31. Kim HJ, Kim JJ, Myeong NR, et al. Segregation of age-related skin microbiome characteristics by functionality. Sci Rep 2019;9:16748.
32. Jugé R, Rouaud-Tinguely P, Breugnot J, et al. Shift in skin microbiota of Western European women across aging. J Appl Microbiol 2018;125:907-16.
33. Shibagaki N, Suda W, Clavaud C, et al. Aging-related changes in the diversity of women's skin microbiomes associated with oral bacteria. Sci Rep 2017;7:10567.
34. Li W, Han L, Yu P, Ma C, Wu X, Xu J. Nested PCR-denaturing gradient gel electrophoresis analysis of human skin microbial diversity with age. Microbiol Res 2014;169:686-92.
35. Huang S, Haiminen N, Carrieri AP, et al. Human skin, oral, and gut microbiomes predict chronological age. mSystems 2020;5:e00630-19.
36. Gueniche A, Benyacoub J, Philippe D, et al. Lactobacillus paracasei CNCM I-2116 (ST11) inhibits substance P-induced skin inflammation and accelerates skin barrier function recovery in vitro. Eur J Dermatol 2010;20:731-7.
37. Kober MM, Bowe WP. The effect of probiotics on immune regulation, acne, and photoaging. Int J Womens Dermatol 2015;1:85-9.
38. Patra V, Gallais Sérézal I, Wolf P. Potential of skin microbiome, pro- and/or pre-biotics to affect local cutaneous responses to UV exposure. Nutrients 2020;12:1795.
39. Marzio L, Cinque B, Cupelli F, De Simone C, Cifone MG, Giuliani M. Increase of skin-ceramide levels in aged subjects following a short-term topical application of bacterial sphingomyelinase from Streptococcus thermophilus. Int J Immunopathol Pharmacol 2008;21:137-43.
40. Maguire M, Maguire G. The role of microbiota, and probiotics and prebiotics in skin health. Arch Dermatol Res 2017;309:411-21.
41. Vollmer DL, West VA, Lephart ED. Enhancing skin health: by oral administration of natural compounds and minerals with implications to the dermal microbiome. Int J Mol Sci 2018;19:3059.
42. Meunier M, Scandolera A, Chapuis E, et al. From stem cells protection to skin microbiota balance: orobanche rapum extract, a new natural strategy. J Cosmet Dermatol 2019;18:1140-54.
43. Liebert A, Bicknell B, Johnstone DM, Gordon LC, Kiat H, Hamblin MR. "Photobiomics": can light, including photobiomodulation, alter the microbiome? Photobiomodul Photomed Laser Surg 2019;37:681-93.
44. Yoshimoto S, Loo TM, Atarashi K, et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 2013;499:97-101.
45. Arthur JC, Perez-Chanona E, Mühlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012;338:120-3.
46. Mrázek J, Mekadim C, Kučerová P, et al. Melanoma-related changes in skin microbiome. Folia Microbiol (Praha) 2019;64:435-42.
47. Nakatsuji T, Chen TH, Butcher AM, et al. A commensal strain of Staphylococcus epidermidis protects against skin neoplasia. Sci Adv 2018;4:eaao4502.
48. Wang Z, Choi JE, Wu CC, Di Nardo A. Skin commensal bacteria Staphylococcus epidermidis promote survival of melanocytes bearing UVB-induced DNA damage, while bacteria Propionibacterium acnes inhibit survival of melanocytes by increasing apoptosis. Photodermatol Photoimmunol Photomed 2018;34:405-14.
49. Tang Y, Chen Y, Jiang H, Robbins GT, Nie D. G-protein-coupled receptor for short-chain fatty acids suppresses colon cancer. Int J Cancer 2011;128:847-56.
50. Archer SY, Meng S, Shei A, Hodin RA. p21(WAF1) is required for butyrate-mediated growth inhibition of human colon cancer cells. Proc Natl Acad Sci U S A 1998;95:6791-6.
51. Salava A, Aho V, Pereira P, et al. Skin microbiome in melanomas and melanocytic nevi. Eur J Dermatol 2016;26:49-55.
52. Wood DLA, Lachner N, Tan JM, et al. A natural history of actinic keratosis and cutaneous squamous cell carcinoma microbiomes. mBio 2018;9:e01432-18.
53. Madhusudhan N, Pausan MR, Halwachs B, et al. Molecular profiling of keratinocyte skin tumors links Staphylococcus aureus overabundance and increased human β-defensin-2 expression to growth promotion of squamous cell carcinoma. Cancers (Basel) 2020;12:541.
Cite This Article
Abadías-Granado I, Sánchez-Bernal J, Gilaberte Y. The microbiome and aging. Plast Aesthet Res 2021;8:27. http://dx.doi.org/10.20517/2347-9264.2020.199
Abadías-Granado I, Sánchez-Bernal J, Gilaberte Y. The microbiome and aging. Plastic and Aesthetic Research. 2021; 8: 27. http://dx.doi.org/10.20517/2347-9264.2020.199
Abadías-Granado, Isabel, Javier Sánchez-Bernal, Yolanda Gilaberte. 2021. "The microbiome and aging" Plastic and Aesthetic Research. 8: 27. http://dx.doi.org/10.20517/2347-9264.2020.199
Abadías-Granado, I.; Sánchez-Bernal J.; Gilaberte Y. The microbiome and aging. Plast. Aesthet. Res. 2021, 8, 27. http://dx.doi.org/10.20517/2347-9264.2020.199
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