Topographical diversity of common skin microflora and its association with skin environment type: An observational study in Chinese women

Abstract

This study evaluated cutaneous microbial distribution, and microbial co-occurrence at different body sites and skin environments in Chinese women (39.6 ± 11.9 years, N = 100) during the winter season. Microbial distribution (Propionibacterium acnes, Staphylococcus aureus, Staphylococcus epidermidis, Lactobacillus, Pseudomonadaceae, and Malassezia furfur), association with biomarkers (antimicrobial peptides: LL-37, β-defensins [HBD-2, HBD-3]), and claudin-1) and skin biophysical parameters (transepidermal water loss, pH, skin scaliness and roughness, sebum and hydration levels) were also determined. Skin sites (glabella [GL], hand-back [HB], interdigital web-space [IS], antecubital fossa [AF], volar forearm [VF], back [BA]) were classified as normal, oily or dry based on two-step cluster analysis and exposed or unexposed (uncovered or covered by clothes, respectively) based on seasonal apparel. Pseudomonadaceae and Staphylococcus aureus had the highest and lowest detection rate respectively at all sites. Cluster analysis identified skin sites as 'normal' (HB, BA, AF, VF), 'dry' (IS) and 'oily' (GL). Bacterial alpha diversity was higher in exposed (HB, IS, and GL) compared with unexposed sites (BA, AF and VF). Co-occurrence of Staphylococcus aureus with any of the other five microorganisms was lower in dry and oily skin versus normal skin. Skin exposure, biophysical/barrier profile and biomarkers were found to be associated with bacterial distribution and co-occurrence.

Figure 1

Comparison of dermal health grading of exposed and unexposed sites by dermatologist. (a) Skin aesthetics, and (b) Skin tolerance. Abbreviations: AF, antecubital fossa; BA, back; GL, glabella; HB, hand-back; IS, interdigital web space; VF, volar forearm. Boxed sites represent exposed skin sites.

Figure 2

Participants perception of skin concerns at different skin sites. Abbreviations: AF, antecubital fossa; BA, back; GL, glabella; HB, hand-back; IS, interdigital web space; VF, volar forearm.

Figure 3

Differentiation of skin sites by cluster analysis based on moisture, sebum and transepidermal water loss. Blue, normal skin; red, oily skin; green, dry skin; skin sites (GL, HB, IS, AF, VF, BA) were classified as normal (HB, BA, AF, VF), oily (GL) or dry (IS) based on two-step cluster analysis and as exposed (HB, IS, GL) or unexposed (BA, AF, VF) based on seasonal apparel (exposed, uncovered by clothes/exposed to UV radiations during study period; unexposed, covered by clothes/ without direct UV exposure during study period). (a) Cluster analysis was based on three parameters (moisture, sebum and TEWL) and classified the three skin types with respect to these parameters. Coloured points representing skin types on the cluster plot denote the relative moisture, sebum or TEWL. The high TEWL values represents higher water loss and weakening of the skin barrier; higher sebum values are associated with higher oiliness of the skin. (b) Percentages given in the rows denote the distribution of every skin site to three model-generated skin groups among all participants. Each group (column) included some dominant skin sites (highlighted). (c) Considering the location and characteristic of the 6 skin sites, three model-generated skin groups are named as “Normal”, “Dry” and “Oily” skin sites. In each group, sites can also be classified into whether the site is exposed to UV radiations or covered by clothes to prevent UV radiations (un-exposed). Abbreviations: AF, antecubital fossa; BA, back; GL, glabella; HB, hand-back; IS, interdigital web space; TEWL, transepidermal water loss; VF, volar forearm.

Figure 4

Network analysis (a) Association between site exposure dependent skin microflora distribution, biophysical parameters and biomarkers (by logistic regression); (b) Physiology dependent with other physiology parameters, microflora, and biomarkers in every skin type (by linear regression). Each node represents bacteria/fungi, the colour of the nodes corresponds to the unexposed site (cyan), exposed site (pink), normal skin site (dark blue), oil skin site (red), and dry skin site (yellow). Bacteria/microorganism are represented as circle. The size of the node corresponds to the square root of (positive rate) *30. The colour of the edges corresponds to the positive (green) or negative (purple) regression estimated coefficient. The length of the edges has no meaning. Solid line represents p < 0.05 and dotted line represents 0.05 < p < 0.1 Star shape represents biophysical parameters and skin texture index, triangles correspond to biomarkers. The width of arrow between any two elements (circle, triangle and star) represents the quantitative contribution from one element to another element, calculated based on linear regression and logistic regression model. Only significantly contributing elements were included in the figure. Abbreviations: Lactob, Lactobacillus; Malass, Malassezia furfur, SEsc, scaliness; SEr, roughness; TEWL, transepidermal water loss.

Figure 5

Microbial co-occurrence based on i) skin type, normal to dry (a), normal to oily (b) and ii) skin exposure (c). Dots represent the co-occurrence percentage difference between two given microorganisms when comparing one skin type with another, at the intersection of row and column. Red denotes decreased co-occurrence percentage compared to normal (versus dry, ‘a’; and versus oily ‘b’) and unexposed (versus exposed, ‘c’) sites. Green denotes increase. e.g., the co-occurrence rate between S. aureus and the five studied microorganisms decreased, while the co-occurrence rate between S. epidermis and Pseudomonadaceae increased. The more negative the value, the weaker is the co-occurrence e.g., the value −10.334 represents relatively lower co-occurrence of Pseudomonadaceae and S. aureus at exposed sites versus unexposed sites, while the value 17, represents relatively higher co-occurrence of Pseudomonadaceae and S. epidermis at exposed sites versus unexposed sites. Co-occurrence rate = (the total number of studied sites with two co-occurring microorganism + the total number of studied sites with neither of two co-occurring microorganism)/total number of studied sites.