Skin Microbiome As Years Go By

American Journal of Clinical Dermatology (2020) 21 (Suppl 1):S12–S17 https://doi.org/10.1007/s40257-020-00549-5 REVIEW ARTICLE Skin Microbiome as Years Go By Paula Carolina Luna1 Published online: 10 September 2020 © The Author(s) 2020 Abstract The skin microbial communities, i.e., the microbiota, play a major role in skin barrier function so must remain dynamic to adapt to the changes in the niche environment that occur across the diferent body sites throughout the human lifespan. This review provides an overview of the major alterations occurring in the skin microbiome (microbial and genomic components) during the various stages of life, beginning with its establishment in the frst weeks of life through to what is known about the microbiome in older populations. Studies that have helped identify the factors that most infuence skin microbiome function, structure, and composition during the various life stages are highlighted, and how alterations afecting the delicate balance of the microbiota communities may contribute to variations in normal physiology and lead to skin disease is discussed. This review underlines the importance of improving our understanding of the skin microbiome in populations of all ages to gain insights into the pathophysiology of skin diseases and to allow better monitoring and targeted treatment of more vulnerable populations. 1 Introduction Key Points The skin is the largest organ of the human body and is Studies of the cutaneous microbiome (microbial and colonized by highly variable microbial communities, genomic components) across diferent age groups have referred to as the microbiota, that are infuenced by multi- highlighted the dynamic nature of the skin microbial ple factors. Diferent communities with distinct functions communities (the microbiota), beginning during the are present in the epidermal and dermal compartments, very early stages of life following initial exposure to the with the environment having a broader impact on the maternal microbiome and continuing with shifts in com- microbiota of the outermost layers of the epidermis [1, munity structure and diversity through to old age. 2]. Skin-resident microbes contribute to the establishment Beyond the frst few weeks of life, body site is a major of cutaneous homeostasis and can modulate infammatory determinant of skin microbiome structure and diversity, responses or trigger pathogenicity depending on the host but many other factors that infuence these site-specifc context [3]. The mutualistic relationship between micro- communities during the diferent stages of life have been bial communities and the host is essential for establish- identifed, with some alterations potentially being associ- ing the well-controlled and delicate balance needed for ated with skin disease. healthy skin. The skin microbiota plays a major role in the function of the skin as a barrier against environmental Understanding the skin microbiome at all stages of life threats and infections. To fulfll this role, the microbiota is important for determining the impact of early altera- remains dynamic throughout the human lifespan. Although tions in the microbiome on future health, gaining a better the skin microbiome, comprising microbial and genomic understanding of the pathophysiology of skin diseases, components, has been well studied in adults [1, 2, 4–7], and aiding the development of age-adapted treatments. less information is available in children and the elderly. This article provides an overview of current knowledge on the main changes occurring in the skin microbiome throughout the diferent life stages, focusing on the epider- * Paula Carolina Luna [email protected] mal microbiome, which is the most exposed to surrounding factors and is more diverse and varying than the der- 1 Hopital Alemán, Pueyrredón Av 1640, mal microbiome [1]. This knowledge is key for enabling C1118 AAT Buenos Aires, Argentina Vol:.(1234567890) Skin Microbiome as Years Go By S13 the dermatologic specifcities and needs of each age group very early in life, before the infant has had extensive contact to be better addressed. with other environmental sources of microorganisms. In preterm infants, physical and functional diferences in the immature skin may alter the resident microbiome compared with that of full-term infants. Pammi et al. [11] found 2 Settlement at Birth that overall skin bacterial richness (variety of species) and evenness (i.e., the relative abundance of the community) Birth marks a time of drastic change for the skin of the tended to be lower in preterm infants than in term infants, newborn as it undergoes a sudden transition from an with no diferences in richness or composition between sur- almost bacteria-free aqueous environment to an atmos- veyed skin sites observed in either group within the frst pheric one with constant exposure to microbes. Immedi- 4 weeks of life. However, a trend was observed for increas- ately after birth, fetal skin is colonized by surrounding ing microbial diversification with increased gestational microorganisms. These microorganisms have been shown age at baseline and then during the frst 4 weeks of life for by Dominguez-Bello et al. [8] to difer according to the both preterm and term neonates. Comparisons of bacterial mode of delivery: the cutaneous bacterial signature (com- composition revealed that Firmicutes (predominant genus munity diversity and structure) of vaginally delivered neo- Staphylococcus) were more abundant and Proteobacteria nates resembles the mother’s vaginal bacteria, with Lacto- less abundant in preterm neonates than in term neonates. bacillus predominating, whereas that of neonates delivered At 4 weeks after birth, the skin microbiome of the preterm by cesarean resembles the cutaneous bacteria, including infants did not difer according to the mode of delivery, simi- Staphylococcus, Corynebacterium, and Cutibacterium lar to previous fndings in term neonates [10], but was found (formerly Propionibacterium [9]). Furthermore, unlike to be altered by antibiotic exposure [11]. In preterm infants, their mothers, neonates have been shown to harbor bacte- immaturity of the skin structure and appendages, as well as rial communities that are undiferentiated across multiple the hospital environment, may explain the decreased skin body habitats (skin, oral, nasopharyngeal, gut, vagina, microbial diversity (richness and evenness) as compared etc.), regardless of the delivery mode [8, 10]. The vertical with term neonates, and partly explain the existence of ges- transmission of the vaginal microbiota from the mother tational age-dependent diferences. Comorbidities, includ- to her baby may serve an initial defensive role in neona- ing respiratory illness, sepsis, necrotizing enterocolitis, and tal skin. Conversely, reduced skin microbial diversity has invasive clinical procedures, may also afect the developing been reported in neonates born by cesarean delivery [10]. skin microbiome. This reduced diversity, combined with the lack of exposure The frst exposure of neonates to the vaginal microbiota to vaginal bacteria, may lead to delayed development of appears to play an important role in the initial establishment the nutritional and immune functions associated with the of the cutaneous microbiota and may also have an impact microbiota across the diferent body habitats [8], perhaps on further bacterial colonization of the gut and other body in part explaining the greater susceptibility of cesarean- habitats [8]. Diferences in the initial skin microbiome may born infants to certain pathogens and allergies. However, thus have broader impacts on infant health, and on health as cesarean delivery is usually medically indicated, the later in life, and therefore need to be more deeply investi- many potential confounders associated with the need for gated. Interventions aiming to restore the diversity of the this procedure may also have an impact on the microbiome cutaneous microbiome in preterm neonates could also be acquired by the ofspring. Moreover, the skin microbial developed to prevent pathogen colonization and subsequent pattern has been found to difer depending on whether neo- systemic infections in this more vulnerable population [11]. nates were delivered by a labored or an unlabored cesarean [10]. Further analyses indicate that by 4–6 weeks after birth, 3 Infants infant skin microbiome structure and function have already signifcantly expanded and diversifed, with prominent body Gradual maturation of skin microbiome function, structure, site specifcities similar to those of the maternal skin micro- and composition has been shown to continue throughout the biome [10]. For instance, Chu et al. [10] showed that the frst years of life [12]. Large interindividual variations in microbiome of infant skin and nares was characterized by skin bacterial communities, along with tremendous diversity Staphylococcus (Firmicutes) and Corynebacterium (Act- in both community composition and the timing of bacte- inobacteria), as in the mother. This reorganization appeared rial acquisition, have been observed in healthy infants by to be primarily driven by the body site and was no longer Capone et al. [12]. Although data indicate that the number infuenced by the mode of delivery. Hence, site-specifc dif- and type of genera in a specifc skin area do not signif- ferences in skin microbial abundance and structure emerge cantly change over the frst year, the relative abundance of S14 P. C. Luna the community has been reported to increase

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