Color homogeneity and visual perception of age, health, and attractiveness of female facial skin Paul J. Matts, PhD,a Bernhard Fink, PhD,b Karl Grammer, PhD,c and Maria Burquest, BAd Egham, United Kingdom; Göttingen, Germany; Vienna, Austria; and Cincinnati, Ohio Background: Evolutionary psychology suggests that skin signals aspects of mate value, yet only limited empirical evidence exists for this assertion. Objectives: We sought to study the relationship between perception of skin condition and homogeneity of color/chromophore distribution. Methods: Cropped skin cheek images from 170 girls and women (11-76 years) were blind-rated for attractiveness, healthiness, youthfulness, and biological age by 353 participants. These skin images and corresponding melanin/hemoglobin concentration maps were analyzed objectively for homogeneity. Results: Homogeneity of unprocessed images correlated positively with perceived attractiveness, healthiness, and youthfulness (all r [ 0.40; P \ .001), but negatively with estimated age (r = 0.45; P \ .001). Homogeneity of hemoglobin and melanin maps was positively correlated with that of unprocessed images (r = 0.92, 0.68; P \.001) and negatively correlated with estimated age (r = 0.32, 0.38; P \.001). Limitations: Female skin only was studied. Conclusions: Skin color homogeneity, driven by melanin and hemoglobin distribution, influences perception of age, attractiveness, health, and youth. ( J Am Acad Dermatol 2007;57:977-84.) I n recent years, evolutionary psychologists have made considerable efforts to investigate human physical attraction and the influence of appearance on mating decisions. It has been suggested that visible skin condition, particularly that of women, has some signaling value relevant for human mate choice, and men and boys are likely to have evolved preferences for skin that signals youth and health.1-3 From P&G Beauty, Eghama; Department for Sociobiology/Anthropology, Institute for Zoology and Anthropology, University of Göttingenb; Ludwig-Boltzmann-Institute for Urban Ethology, Department for Anthropology, Viennac; and P&G Beauty, The Procter & Gamble Company, Cincinnati.d Supported in full by the Procter & Gamble Company. Disclosure: Dr Matts and Ms Burquest are paid employees of the Procter & Gamble Company. Drs Fink and Grammer have no conflicts of interest to declare. Accepted for publication July 28, 2007. Reprint requests: Bernhard Fink, PhD, Department for Sociobiology/ Anthropology, Institute for Zoology and Anthropology, University of Göttingen, Berliner Strasse 28, D-37073 Göttingen, Germany. E-mail: bernhard.fink@ieee.org. Published online August 24, 2007. 0190-9622/$32.00 ª 2007 by the American Academy of Dermatology, Inc. doi:10.1016/j.jaad.2007.07.040 If this were indeed true, it would offer another explanation as to why women place such an importance on the condition of their skin and its refinement through, for example, cosmetic products and procedures. Although some studies have investigated the perception of apparent skin condition,4,5 little is known about how visual perception of facial skin color distribution relates to its objective analysis. Early attempts to study variation in age perception of male faces as a result of shape and color manipulation revealed that color (ie, red, green, blue) intensity distribution affects perceived age,6 as does the sex and ethnicity of the faces.7,8 These studies, however, did not differentiate between skin pigmentation and age cues that relate to topographic information. Recent evidence demonstrates that skin pigmentation contributes to the neural representation of face identity,9 thus, emphasizing the importance of considering pigmentation cues in facial perception studies. Moreover, there is evidence that people are sensitive to variation in skin color distribution, and that such variationeindependent of surface topography cueseaffects visual perception of female facial attractiveness, healthiness, and age. Fink et al10 note that the dynamic range of estimated ages of female 977 978 Matts et al J AM ACAD DERMATOL DECEMBER 2007 faces, on the basis of skin color evenness alone, can account for up to 20 years of apparent age, and that even skin color distribution is perceived as healthy and beautiful. In view of new measurement capabilities and a growing understanding of the relationship between skin biology and optics, it seems timely to take a more detailed look at which skin components, responsible for color distribution, specifically drive this observed variance in visual perception. Indeed, one shortcoming of available psychobiological studies on the effect of skin condition on facial perception and judgment is that, to date, it appears that a foundational approach to cutaneous optics has not yet been considered. A modern understanding of cutaneous optics is based largely on the development of increasingly sophisticated mathematic models to explain the interaction of light with skin. A review of these models11-20 reveals that normal human skin coloration is driven overwhelmingly by only 3 components, that is, absorption (and associated spectral modification) by the melanin and hemoglobin chromophores and subsurface scattering by collagen. It follows, therefore, that the kaleidoscope of both interindividual and intraindividual skin coloration is derived solely from specific blends of these 3 optical components. Understanding how the expression and presentation of these molecules change with age, therefore, is critical in truly understanding the changing appearance of skin across a human lifetime. In a previous study, we showed that in Caucasian skin, skin color evenness within whole, stimulus faces was an important subjective visual cue, coding for youth, health, and attractiveness.10 Here we report the results of a study on visual perception of isolated fields of skin, cropped from images of female faces and relate the perception of these images to: (1) an objective analysis of homogeneity of skin color; and (2) gray-scale concentration maps of melanin and hemoglobin in the same image and obtained using a new technique. Our aim was to investigate the relative contributions of chromophore molecules to the apparent decreasing color homogeneity/increasing perceived contrast of aging human female skin and relate these findings to visual perception and judgment of age, health, and attractiveness. METHODS Institutional review board approval Study approval was granted by the corporate institutional review board. Stimulus material A total of 170 British women and girls from the ages of 11 to 76 years (mean age = 37.39, SD = 17.35) was recruited and photographed from the left profile. This was achieved using a custom digital imaging rig comprising a 6.2-megapixel digital single-lens reflex camera fitted with a 45-mm 1:2.8P lens (Nikon Corp, Tokyo, Japan), a fully cross-polarized multiple flash lighting system, and a chin rest to ensure accurate, reproducible positioning of individuals and overall component stability. Full cross-polarization of the light source was used to effectively eliminate visible high-frequency/low-amplitude skin surface topography (microtexture). Images were captured and stored in uncompressed tagged image file format (.TIFF) format at a resolution of 3277 3 2226 pixels and 72 dots per inch (dpi). No color correction or spatial filtering was applied to these images. We obtained a total of 170 skin cropped samples from the left hemiface. These samples represented regions of interest with a size of 500 3 500 pixels at 72 dpi and were taken from the same region of each face (Fig 1). The cheek area sampled was chosen as it was generally devoid of high-amplitude, lowfrequency features (eg, lines, wrinkles, furrows) that would have contributed significantly to visible contrast. Although the extraction of image samples was done automatically, some had to be adjusted slightly (ie, moved to the left or right along the x-axis) when the selected region was partly covered by hair or included facial topography cues. Rating study A rating study was carried out using computers (Macintosh, Apple Computer, Cupertino, Calif) connected to color-corrected monitors (LaCie electron 19blue IV, LaCie, Hillboro, Ore) set to a resolution of 1600 3 1200 pixels. Monitors were calibrated before the study with the aid of blue eye calibrators (LaCie) to ensure constant color conditions and resolution for all participants. A rating software solution was implemented on a central computer server using hypertext preprocessor programming language and rating took place at two locations (Vienna, Austria, and Göttingen, Germany). A total of 353 participants (127 male and 226 female members of the public) between the ages of 12 and 57 years (mean age = 22.82, SD = 4.52) rated the stimuli. They were presented randomly on the screen and each participant rated 10 randomly selected skin image samples. Participants were requested to estimate the biological age of the individual from which the corresponding skin image sample had been taken using a single-step scale ranging from 10 to 60 years. In addition, participants were asked to rate each skin image for perceived attractiveness, healthiness, and youthfulness using a 10-point rating (1 = not at all, 10 = highly). J AM ACAD DERMATOL Matts et al 979 VOLUME 57, NUMBER 6 Fig 1. Examples of original cropped, cross-polarized digital images (500 3 500 pixels, 72 dpi) taken from left cheek of two individuals (A and B) and corresponding melanin (C and D) and hemoglobin (E and F) chromophore gray-scale concentration maps. A, Real age = 53 years, estimated age (mean) = 49 years. B, Real age = 13 years, estimated age (mean) = 21 years. Chromophore mapping We used a new measurement capability, spectrophotometric intracutaneous analysis (SIA)scopy,21-25 developed by Cotton and Claridge21 and then Astron Clinica (Cambridge, United Kingdom), which operates on the principle of chromophore mapping, that is, the in vivo measurement of the concentration and distribution of eumelanin, oxyhemoglobin, and dermal collagen, to produce mutually exclusive grayscale concentration maps of these chromophores. The technique is based on a unique combination of epiluminescence microscopy, contact remittance spectrophotometry, and hyperspectral imaging. More recent research by Astron Clinica has yielded noncontact SIAscopy that overcomes the limitations of a skin contact probe.25,26 Noncontact SIAscopy uses a conventional, although finely calibrated, digital camera and lighting system and may be used to acquire large-field melanin and hemoglobin chromophore maps. All optical components of the imaging system used in this study, ie, the camera charged coupled device (CCD), the flash source, and polarizing filters had, therefore, been previously calibrated by Astron Clinica to facilitate noncontact SIAscopy and the construction of noncontact melanin and hemoglobin chromophore concentration maps. In addition to the full-color TIFF files, images were also saved out in Fuji’s proprietary CCD-.RAW 12-bit file format (Fuji, Tokyo, Japan). Custom SIA algorithms batch-processed the CCD-.RAW files to produce melanin and hemoglobin gray-scale concentration maps giving 256 possible concentrations of melanin and hemoglobin (where 0 [darkest gray scale] = highest chromophore concentration and 256 [lightest gray scale] = lowest chromophore concentration). Although, therefore, the output of this method represented chromophore concentration maps, they were also gray-scale images in portable network graphics (.PNG) format, available to image analysis techniques (Fig 1). Image analysis of skin and chromophore maps Image homogeneity can be evaluated qualitatively as having one or more of the following properties: fineness, coarseness, smoothness, granulation, randomness, lineation, mottled, irregular, or hummocky.27 Although there are many statistical approaches to the characterization and measurement of image homogeneity, the co-occurrence approach has produced the best results in previous studies.28 The power of the co-occurrence approach is in its characterization of the spatial interrelationships of gray tones in a textural pattern.29,30 Co-occurrence matrices are based on secondorder statistics, which are the spatial relationships of pairs of pixel gray values in digital images and operate by counting how often pairs of gray levels of 980 Matts et al J AM ACAD DERMATOL DECEMBER 2007 RESULTS Fig 2. Scatterplot with regression lines of associations between estimated biological age and mean ratings of appearance attributes. pixels (which are separated by a certain distance and are along a certain direction) occur in a digital image of texture. Co-occurrence matrices are not used directly, but features based on them are computed so that characteristics of textures, such as homogeneity, coarseness, and periodicity are captured. In a classic article on this subject, Haralick et al31 suggested 14 texture operators (most of them are highly interrelated). Of the original features of Haralick et al,31 we chose one operatore‘‘homogeneity’’ethat produced the best results in past studies and that was, therefore, used most frequently4,29-32: Homogeneity ¼ + + i j 1 pði; jÞ 11ji jj Where i and j are gray-scale values in rows and columns, and p(i,j) is the frequency of their occurrence. The homogeneity algorithm measures the monotonicity (ie, the closeness of the distribution of elements in the co-occurrence matrix) of an image. A higher value corresponds to a more homogeneous image. Before analysis of the images by co-occurrence matrices, the application of an image-sharpening filter (‘‘Mexican hat kernel’’; for details see Sonka et al33) was used. Image sharpening replaces the central pixel by the average of itself and those in its neighborhood to make edges steeper.34 These neighboring pixels are multiplied by a set of integer weights and, by convention, these are multiplied by pixels surrounding the central pixel. Dividing it by the sum of the positive weights normalizes the sum. This scheme was applied to every pixel of the respective input image. After this procedure, sharpened images were subjected to the homogeneity analysis. Perception of skin images The estimated biological age (ie, the aggregated estimates from all judges) of individuals from corresponding skin image samples ranged from 17.3 to 53.1 years (mean = 32.26, SD = 8.50), a range of some 30 years. There was a significant positive correlation between the actual biological age of the individuals who provided facial images and the corresponding estimated age from their skin image samples (Pearson correlation coefficient r = .612, P \ .001). Significant negative correlations emerged between estimated age and the global appearance attributes (attractive, r = .728; healthy, r = .703; youthful, r = .946; all P \ .001) (Fig 2). Moreover, correlations with these attributes were also found significant throughout with actual biological age (attractive, r = .390; healthy, r = .400; youthful, r = .583; all P \ .001). All the Pearson correlations above remained significant after Bonferroni adjustment of alpha level for multiple significance tests. Analysis of skin images Pearson correlation coefficients of the homogeneity descriptor with attributes from the rating study revealed significant correlations throughout in the predicted direction, ie, higher values of skin homogeneity were correlated with higher ratings for attractiveness (r = .395, P \ .001), healthiness (r = .409, P \.001), and youthfulness (r = .493, P \.001) (Fig 3). All correlations remained significant after Bonferroni adjustment of alpha level for multiple significance tests. In addition, homogeneity of the skin image samples correlated significantly and negatively with estimated age of the corresponding individual (r = .454, P \.001). Similar results were obtained for correlations between real age of the individuals and texture descriptors (homogeneity: r = .378, P \.001). Analysis of chromophore maps Two measures of homogeneity of melanin maps were deleted before the analysis as their values exceeded the mean by more than 5 SD. Values of melanin map homogeneity showed some positive skew whereas homogeneity of hemoglobin maps was slightly negatively skewed. We, therefore, applied a square root transformation to these variables to overcome potential statistical bias from large values. Homogeneity of hemoglobin and melanin maps was significantly correlated with those of the original skin images (hemoglobin, r = .918; melanin, r = .677; all P \.001), indicating that the chromophore maps J AM ACAD DERMATOL Matts et al 981 VOLUME 57, NUMBER 6 Fig 3. Scatterplots with regression lines of associations between texture descriptor homogeneity of unprocessed (original) skin images with attributes from rating study. generated in this manner are highly related to the visible color distribution of a woman’s natural skin. Furthermore, estimated biological age of individuals from corresponding skin images correlated significantly and negatively with both homogeneity of hemoglobin and melanin chromophore maps (hemoglobin, r = .323; melanin, r = .380; all P\.001) (Fig 4, A). Similar results with slightly lower correlation coefficients was obtained for the association of melanin but not hemoglobin map homogeneity with actual biological age (hemoglobin, r = .138, P [ .05; melanin, r = .375, P \ .001) (Fig 4, B). Homogeneity of hemoglobin and melanin maps was significantly and positively correlated with perceived attractiveness, healthiness, and youthfulness (Table I). Linear regression analyses, with estimated age of individuals from corresponding skin image samples and actual biological age as dependent variables and homogeneity measures of hemoglobin and melanin chromophore maps as independent variables, revealed overall significant models with melanin, but not hemoglobin, chromophore maps as a significant predictor of both estimated and actual biological age (estimated age: F [2, 167] = 15.64, P\.001; actual age: F [2, 167] = 14.65, P \.001) (Table II). DISCUSSION The highly significant positive correlation between estimated and actual age of the individuals from whom the images were originally taken indicates that we can discern, to a surprising extent, the biological age of an individual, based solely on visible color distribution, even in isolated, noncontextual skin images. Furthermore, our results indicate that variation in facial skin color distributioneindependent Fig 4. Scatterplots with regression lines of associations between image homogeneity of chromophore maps with estimated (A) and actual (B) biological age. of topographic information of the skinesignificantly influences the estimation of a woman’s biological age and judgment of attractiveness, health, and youth, with the skin of younger women being rated more positively. For the first time in our knowledge, we have also related these observations to the molecular basis of visible skin color distribution and found significant correlations with melanin and hemoglobin homogeneity within the same skin regions. Melanin was found to provide the best overall model explaining both biological and perceived age of the skin image samples. Why is visible skin color homogeneity so closely linked to perceived age, health, and attractiveness? We view the world through sensitive visible light meters and, therefore, the phenomenon of contrast sensitivity is of critical importance when considering the perception of chromophore changes in human skin. ‘‘Contrast’’ can be defined simply as the difference between two adjacent luminance values (the perceived intensity of light remitted from an object, not strictly brightness) divided by their sum and 982 Matts et al J AM ACAD DERMATOL DECEMBER 2007 Table I. Pearson correlations (r) of skin image rating values with image analysis output values from chromophore maps Homogeneity Attractiveness Healthiness Youthfulness Hemoglobin Melanin .330* .346* .363* .226y .213y .367* *P # .001. y P # .01. ‘‘contrast sensitivity’’ is the reciprocal of the minimum contrast required for detection of a feature. Put another way, it is a measure of how faded or washed out an image can become before it is indistinguishable from a uniform field. It has been determined experimentally that the minimum discernible difference in gray-scale level that the human eye can detect is about 2% of full brightness.35,36 This outstanding contrast sensitivity allows us to perceive the world around us in great detail; indeed, without contrast (and a means for achieving this by a variable-focus mechanism), we would effectively be rendered blind. The human eye, therefore, is drawn automatically to areas with high differences in adjacent luminanceein simple terms, we view the world through edges created by contrast. Contrast sensitivity is also a function of the size, spatial frequency, or both of the features in the image. Perceived contrast is highest, therefore, when both the difference in adjacent luminance values is high and when associated features are large. In aging human skin, perceived contrast is certainly increased by large differences in adjacent pure luminance values as a result of shadowing formed by high-amplitude/low-frequency surface topography (especially so in the case of linear features such as lines, furrows, and wrinkles). Color, however, also plays a pivotal role. Haralick et al27,31 discuss the concepts of tone (the varying shades of gray within a digital image) and texture (relating to the spatial [statistical] distribution of those gray tones). Although these concepts appear to apply most intuitively to shadow, the luminance variations associated with the perceived intensity of light remitted from chromatic inhomogeneity within a field of vision also contribute significantly to tone, texture, and, therefore, luminance contrast.37 Finally, although luminance is the dominant effect in driving perceived contrast, even in colored fields, the phenomenon of color contrast should also be noted, where adjacent colors of increasing difference in hue angle38 (eg, red-green, blue-yellow) drive a concurrent increase Table II. Linear regressions with estimated and actual biological ages as dependent variables, and homogeneity and contrast measures of hemoglobin and melanin maps as independent variables B Estimated age Homogeneity melanin Homogeneity hemoglobin Actual biological age Homogeneity melanin Homogeneity hemoglobin SE B b 1.914 1.438 .581 .837 .291* .152 5.977 2.417 1.181 1.702 .449* .126 Note: R2 = .16 for estimated age, R2 = .15 for actual biological age. B, unstandardized (regression) coefficient (SE B = std error of B). *P \ .001. in contrast. On this basis, it would be predicted that a red feature would be more clearly perceived than a brown feature against a flesh-colored background (assuming equal size and luminance for each feature). Indeed, we see some evidence for this phenomenon with the relatively greater correlation coefficients for hemoglobin over melanin when chromophore homogeneity and ratings for attractiveness and healthiness are compared (Table I). Understanding the importance of uneven color in driving perceived contrast (whether derived from color or luminance), what is the molecular basis for the increasing color unevenness of aging skin? We need to return to the chromophores responsible for skin color in the first instant. In young, healthy skin, both constitutive and facultative melanin expression is uniform and synchronous, resulting in an extremely homogeneous distribution of the melanin chromophore in both basal skin tone and sunexposed sites. Distribution is so homogenous that skin coloration is essentially featureless, lacking contrast. This situation changes considerably, however, under the influence of so-called photoaging. ‘‘Photoaging’’ is the term given to the superimposition of chronic sun damage on the intrinsic (chronologic) aging process. In contrast with the apparent age-related loss of melanogenic activity in non-sunexposed skin,39 it is now well-established that cumulative lifetime exposure to solar ultraviolet radiation results in a progressive accumulation of mottled hyperpigmentation,40,41 including diffuse hyperpigmentation (the whispy dyspigmentation commonly present on sun-exposed skin, not related to systemic disease20,42) and solar lentigines.20,42-46 In summary, the process of aging and, in particular, photoaging, produces localized concentration and an increasingly heterogeneous distribution of melanin in human skin. J AM ACAD DERMATOL Matts et al 983 VOLUME 57, NUMBER 6 Hemoglobin is confined to membrane-bound red blood corpuscles, which are in turn confined to blood contained within the rich network of blood vessels supplying this organ. Whereas it is generally accepted that intrinsic aging produces a reduction in the superficial horizontal capillary plexus,42,47-49 once again, the vasculature of sun-exposed skin is markedly different. Photoaging results in capillaries that are tortuous and dilated, producing a spectrum of severity of telangiectasia.50,51 Within areas of chronic sun exposure, the vessel wall appears to thicken as a result of the peripheral addition of a layer of basement membranelike material.52-54 A combination of this increased vascular rigidity and a reduction in density of the supportive, perivascular connective tissue produces fragile vessel walls that are less able to support the internal turgor of blood volume and external mechanical stress. As a result of this mechanical failure, chronic dilation, the formation of sinuses and galleries and, to a limited extent, low-grade purpura, drive the progressive and classic appearance of telangiectasia and blotchiness associated with aging skin and, in particular, sun-exposed areas. Importantly, once again, aging produces a steady accumulation of local concentrations of this chromophore in human skin and an associated increase in heterogeneity of hemoglobin-based features, particularly in sun-exposed areas. The process of intrinsic and extrinsic aging, therefore, drives a steady accumulation of enlarging, localized concentrations of the two colored chromophores, melanin and hemoglobin. In other words, independent of contrast formed by shape and/or topography, localized concentration of chromophores in aging skin causes a significant decrease in homogeneity and a corresponding increase in contrast, particularly in sun-exposed areas such as the face, neck, and décolletage. In this context, it should be noted that the current study considers only Caucasian female participants aged 10 to 70 years, living in the United Kingdom and recruited in Reading at 518N and, thus, receiving on average a relatively low cumulative lifetime dose of erythemal ultraviolet radiation. It could be predicted with some certainty, therefore, that if participants had been recruited from Caucasian populations living in lower latitudes (with concomitant higher insolation), the dynamic range of color heterogeneity would be significantly greater, with even higher impact on perception. It is also worth noting that one of the limitations of this study is the use of Caucasian skin types onlyethe study of other skin types presents much scope for future research. 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