Color homogeneity and visual perception of age, health, and

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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
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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).
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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
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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
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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
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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.
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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.
In a recent study10 we showed that, independent
of facial shape, form, or skin topography, uneven
female facial skin coloration is significantly and
positively correlated to perception of age while
significantly and negatively correlated to perception
of health and beauty. In this current study, we build
on these findings and show, for the first time, the
molecular basis for this phenomenonea progressive
decrease in chromophore homogeneity, leading to
an increase in perceived contrast that appears to be
an important visual cue for the judgment of age,
health, and attractiveness.
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