DOI: 10.1111/j.1600-0625.2012.01545.x
Viewpoint
www.blackwellpublishing.com/EXD
‘Nosing Around‘ the human skin: What information is concealed in
skin odour?
Stefan Kippenberger1, Jan Havlı́ček2, August Bernd1, Diamant Thaçi1, Roland Kaufmann1 and
Markus Meissner1
1
Department of Dermatology, Venereology and Allergy, Johann Wolfgang Goethe University, Frankfurt/Main, Germany; 2Department of
Anthropology, Faculty of Humanities, Charles University, Prague, Czech Republic
Correspondence: Stefan Kippenberger, Department of Dermatology, Venereology and Allergy, Johann Wolfgang Goethe University, Theodor-SternKai 7, D-60590 Frankfurt/Main, Germany, Tel.: +49 69 6301 7734, Fax: +49 69 6301 6466, e-mail: [email protected]
Abstract: In today′s world, natural body odour is mostly
considered as being unpleasant and combated by intensive
cleansing, deodorants and perfumes. However, there is evidence
that volatile body compounds provide the recipient with
important information. Here, we present the chemical identity
of odorous compounds derived from odourless precursors
within sweat and sebum. Moreover, distinct volatile markers
may be relevant for the clinical diagnosis of disease.
Interestingly, ageing seems to correlate with the appearance of
specific compounds that convey the so-called old man smell.
Finally, it is discussed if human skin odour has the quality to
act as pheromone transmitting information between individuals
in terms of major histocompatibility complex type or
reproductive status.
Skin Odour: nothing is more remarkable than a
smell!
In addition to apocrine glands, the eccrine sweat glands also
contribute to skin odour. They are distributed all over the skin
but particularly concentrated in the soles of the feet, the palms of
the hands and the forehead. Eccrine sweat is mostly water, but
also contains glycoproteins, lactic acid, sugars, amino acids and
electrolytes (12) providing an ideal substrate for the growth of
microorganisms. The sebaceous gland is also considered to be a
player in skin odour formation. It was found that yeasts of the
genus Pityrosporum when grown on a lipid substrate similar to
human sebum produce c-lactones recognized as having a fruity
canned-peach odour (13). In particular, Pityrosporum ovale, the
most frequent microorganism of the capillitium (14), may contribute to the typical human scalp odour, which is significant in
smell recognition of newborns. Furthermore, it is speculated that
human sebum acts as a concrete, a carrier compound that retards
the liberation of odorous molecules (15).
Because of the diverse composition of odour producers within
human skin, different body areas such as scalp, axillae or feet emit
a specific smell which in toto generates a complex mixture of
odorants. Tracking dogs, for example, trained to recognize a person′s scent on a garment worn on a particular body part are not
reliably able to relate the person′s odour to other body parts (16).
The sources of skin odour contributing to an individual ‘odour
signature’ are diverse. A chief producer is the apocrine gland,
located in the axillary, groin and anogenital regions, as well as in
the umbilicus, eyelid (Moll’s glands), areola and the external auditory meatus. They are fully developed up to reproductive maturity.
The characteristic odour of anatomic sites rich in apocrine glands
is formed from the interaction between odourless (water soluble)
precursor molecules found in the glands secretion and the cutaneous microflora (1,2). In particular, aerobic Corynebacteria metabolize odourless steroids producing 16-androstenes (5a-androstenol,
5a-androstenone) with a pungent musk- and urine-like odour (3).
It is, therefore, not surprising that men have been reported to have
more numerous and larger apocrine glands than women (4). Correspondingly, axillary androstenone levels are much higher in men
than in women (5). Moreover, volatile C6-C11 acids, the most
prominent being 3-methyl-2-hexenoic acid (3M2H), are reported
to contribute to axillary malodour (6). Interestingly, 3M2H is
bound to carrier proteins (ASOP1, ASOP2) after secretion into the
apocrine glandular lumen preventing the formation of smell. The
characteristic goat-like axillary odour only appears after liberalization by bacteriolysis (7,8). There are also indications for a genderspecific odour signature: a cheesy, rancid odour derived from the
metabolism of glutamine conjugates seems typical for men,
whereas an onion-like smell from that of sulphur-rich conjugates
seems typical for women (9). Very recently, it was found that a
single nucleotide polymorphism (538G->A) in the gene ABCC11 is
responsible for the transition from a strong axillary odour, as commonly present in Caucasians and Africans, to a faint acidic scent
typical for Asians (10). Interestingly, this nucleotide substitution
correlates with a white and dry earwax phenotype frequently (80–
95%) seen among East Asians and being rare (0–3%) in populations from European and African origin (11).
ª 2012 John Wiley & Sons A/S
Experimental Dermatology, 2012, 21, 655–659
Key words: body odour – pheromone – chemosignalling – behaviour –
ageing – disease
Accepted for publication 24 May 2012
Olfactory perception: smells like a disease
In times where the diagnostic arsenal of physicians was rather limited, patients′ odour served to identify ailments. The diagnosis by
smell goes back to the observations of Hippokrates (460 BC – 370
BC), the famous physician of Ancient Greece, and was carried forward by Galenus (ca. 120 – 200) and Avicenna (980–1037). By
mistake, in the Middle Ages, the smell itself was considered to be
the cause of the disease resulting in the misguided attempts to
combat diseases such as plague and typhus by carrying scented
pouches or torches (17). It is not within the scope of this review
to give a complete list of diseases associated with odour changes;
instead, we would like to focus on some selected examples (see
655
Kippenberger et al.
Table 1). For more detailed information please refer to the recent
review by Shirasu and Touhara (32). For the dermatologist, the
odour emitted by chronic wounds such as ulcus cruris provides
clues about microbial colonization and hence the necessity for an
antiseptic treatment which is reported to have a deodorizing effect
(33). Moreover, bullous congenital ichthyosiform erythroderma,
caused by mutations in keratins 1 and/or 10, is associated with a
foul skin odour (34); however, this criterion plays a minor part in
diagnosis. Interestingly, animals are also reported to be useful in
making a diagnosis by olfactory perception. Inspired by anecdotal
findings where dogs, whose olfactory sensitivity is much superior
to humans, alerted their owners to skin lesions that later became
diagnoses such as melanoma (35) and basal cell carcinoma (36),
more controlled studies were initiated. Recently, it was reported
that a trained Labrador retriever accurately identified cancer
patients by sniffing exhaled breath and stool samples (37). Besides
the use of dogs, also an electronic nose, originally designed to
monitor the air quality, was experimentally used to discriminate
cancer cells in vitro (38). Moreover, the electronic nose is particularly useful to detect odours caused by pathologic microorganisms
such as Helicobacter pylori (39).
The smell of old age
It is a common experience that body odour seems to change not
only from childhood to puberty but also from middle ages to
older age. The so-called ‘old lady smell’, ‘old man smell’ or ‘old
person smell’ is an idiom often used to describe an odour that is
characteristically associated with the elderly. Decreased androgen
production at an older age may contribute to a change in skin
odour as the metabolic activity of apocrine and sebaceous glands
is under control of androgenic hormones (40). Age-related
changes can be perceived by others; the odour of postclimacteric
women was frequently mistaken for that of men. On the other
hand, unfamiliar smellers after being exposed to the same odours
reported feeling relaxed (41). In an analytical study to identify volatile organic compounds that correlate with age using gas chromatography, three compounds (dimethylsulphone, benzothiazole and
nonanal) were found to correlate with age (42). Interestingly, this
extensive study failed to detect the unsaturated C9 aldehyde,
Table 1. Metabolic and infectious diseases with typical odour
Disease
Metabolic
Phenylketonuria
Isovaleric acidemia
Methionine
malabsorption
syndrome
Hypermethioninemia
Trimethylaminuria
Maple syrup urine
disease
Diabetes (particularly
type I)
Infectious
Yellow fever
Typhoid fever
Tuberculosis
Pneumonia
Diphtheria
Cholera
656
Odour quality
References
Musty sweat/urine odour
Cheesy, like sweaty feet
Burnt sugar-, oast house-, celery-like
urine odour
(18)
(19)
(20)
Sulphur-type odour
Rotten fish odour in urine/sweat/
breath/saliva/semen
Caramelized sugar-like sweat/urine/
cerumen odour
Acetone breath/urine odour
(21)
(22, 23)
Butcher′s-shop-like skin odour
Musty or like freshly baked brown
bread body odour
Foul breath
Foul breath
Sweetish, putrid body odour
Fishy stool odour
(28)
(28)
(24–26)
(27)
(29)
(28)
(30)
(31)
2-nonenal, which was reported by a Japanese group to increase
with age (43). Haze et al. found a rapid increase of 2-nonenal in
individuals older than 39 years. The compound was perceived to
smell of orris, fat and cucumber. As in the first study mainly Caucasians participated, it seems likely that the conflicting data may
be diet-linked reflecting a cultural phenomenon. Previous studies
showed that diet can affect the perception of human body odour
(44). For instance, consumption of red meat decreased the pleasantness′ of axillary odour (45). Unfortunately, the Japanese study
does not tell us anything about the eating habits of the individuals
tested; however, in this study, they found the x7 monounsaturated acid, palmitoleic acid, which is a common constituent of fish
oil (46), to be the origin of 2-nonenal. This supports the assumption that a specific diet is the cause of the occurrence of culturespecific odour compounds – also in old age. Furthermore, there is
evidence that the occurrence of age-specific compounds in elderly
persons is caused by lipid peroxidation of higher molecular weight
unsaturated acids, which seems to be upregulated in older individuals (47,48). However, changes in physical activity, frequency and
intensity of personal hygiene measures and changes in grooming
habits with age may also contribute to the occurrence of an agerelated odour.
Communication via pheromones – also in humans?
The term pheromone is a neologism composed of the Greek
words pherein (transfer) and hormone (excite) (49). Karlson and
Lüscher define pheromones ‘as substances which are secreted to
the outside by an individual and received by second individual of
the same species, in which they released a specific reaction, for
example, a definite behaviour or a developmental process’. A third
class, so-called information pheromones, has since been defined to
describe substances that indicate the identity or territory of an
animal (50). First described in insects, pheromones were also
reported in mammals. In mice, for example, a complex mixture of
volatile compounds within urine contributes to pheromonal communication affecting reproduction. Particularly, the major urinary
proteins (MUPs), components of adult male urine, bind to volatile
pheromones and regulate their release into the air from urine
marks. MUPs are involved in a plethora of reactions including
synchronization of ovulation in a group of anoestrous female animals (‘Whitten effect’) and puberty acceleration in juvenile
females (51). Of note, humans seem to be the only mammals with
no active MUP genes yet analysed (52).
Now, we will focus on the evidence for human chemical communication in various social domains. The most often referred
example of human pheromones is menstrual synchrony. It was
initially found in the early 1970s that female students sharing
apartments tend to synchronize the onset of their menstrual cycle
(53). Subsequently, this phenomenon was tested in several dozen
highly variable samples ranging from women sharing offices (54),
basketball players (55), lesbian couples (56) or Bedouin mother–
daughter dyads (57) showing a mixed pattern of results. It was
suggested that time spent together, emotional closeness and cycle
regularity can modulate cycle synchrony (58). Martha McClintock
(53) in her pioneering study speculated that menstrual synchrony
could be driven by chemicals produced in female armpits. This
was originally tested (59), but the study was methodologically
flawed (60). More recently, Stern and McClintock (61) collected
odourless fluids derived from the axillae of women in the late
ª 2012 John Wiley & Sons A/S
Experimental Dermatology, 2012, 21, 655–659
‘Nosing Around‘ the human skin
follicular phase of their menstrual cycle. It was found that exposure to recipient women shortened their menstrual cycle and
accelerated the preovulatory surge of luteinizing hormone (LH).
Leaving aside that the chemicals responsible for the effect are not
known, it should be pointed out that a majority of the studies on
synchronization was criticized for methodological flaws especially
concerning how synchrony was computed (60,62).
Moreover, it is not clear what would be the functional significance of such a phenomenon, although it could have evolved in a
context of different mating systems (e.g. polygyny) in our ancestors and was simply not selected out in recent human populations.
It is thought that in some polygynous mating systems, male mating capacities are restricted. Thus, women might compete for
access to men which in turn can result in oestrous synchrony.
However, evidence for menstrual cycle synchrony in polygynous
primates is equivocal (63).
There are also clues for olfactory communication between both
sexes. In an experiment similar to the above, it was found that
underarm secretions from men have the ability to stimulate the
onset of the next peak of LH (64). Furthermore, such stimulation
has an effect on the emotional state by reducing tension and
increasing relaxation. Another approach was taken by scholars
inspired by analytical studies. As mentioned previously, human
axillary odour is partly due to the presence of some 16-androstenes (primarily 5a-androstenol, 5a-androstenone and androstadienone) that were originally found to affect mating behaviour in
pigs (65). Some authors found a more positive perception of photographs impregnated with the androstenol (66) or a higher number of social interactions (67). On the other hand, after
application of androstenol and androstenone, male participants
found themselves less attractive (68) and other studies reported
no effect (69). More consistent results come from studies employing androstadienone as a stimulus. This steroid was reported to
affect mood, psychophysiology (e.g. skin conductance), cortisol
levels and social perception especially in women (for review see
70). However, it seems that in humans, the reaction to an olfactory stimulus is rather dependent on the context and so goes far
beyond the original pheromone definition (i.e. pheromonal stimulus is followed by a specific behavioural reaction). Interestingly, a
context which would most closely resemble pheromonal effects
according to the original definition is the interaction between a
mother and her newborn baby. Newborn infants when placed on
mother’s stomach spontaneously crawl to the breasts guided by
the sense of smell (they do not show such behaviour when the
areolas are washed) (71). Preference for odour of lactating breast
was observed even in babies fed on formula, suggesting that the
preference is not dependent on previous reward reinforcement
(72). Furthermore, a recent detailed examination of areola morphology shows that a higher quantity of areolar skin glands is
associated with faster onset of breastfeeding and sucking activity
(73).
Skin odour as a mating marker
Sexual selection theories commonly propose mate preferences
based on two different systems: (i) gene products reflecting
quality of the organism; and (ii) complementary genes. In the
first case, frequently referred to as honest signals, it is expected
that a majority of the population would follow such a preference
(74). An example from human odour studies is a preference for
ª 2012 John Wiley & Sons A/S
Experimental Dermatology, 2012, 21, 655–659
odour of individuals with low fluctuating asymmetry (FA) (75).
The level of FA reflects randomly distributed deviations from
perfect bilateral symmetry. As traits on both sides of the body
are based on the same genetic make-up, it is thought that individuals with low-level FA have more finely tuned coordination of
the developmental machinery, and in consequence, they are also
able to cope with environmental stress such as pathogens or toxins (76). In contrast, in the case of preferences for complementary genes, individuals are expected to vary in their preferences
based on their own genetic make-up. One of the most widely
studied models of the preference for complementarity are genes
of the major histocompatibility complex (MHC) (77). Genes of
this complex show high diversity, reaching over 200 different
alleles in some loci in humans. Products of the MHC genes play
a central role in immune system functioning as they specifically
bind peptides of foreign origin and present them on the cell surface to other elements of the immune system (78). High diversity
of the MHC genes is usually explained as a result of balancing
selection and sexual selection (79). As inheritance of the MHC
alleles is co-dominant, offspring of parents with different alleles
show immune responses to wider spectrum of infections. One
can, therefore, expect preferences for individuals of different
MHC profile than ones own. Following pioneering work by
Yamazaki et al. (80) who found that mice prefer odour of conspecifics different in the MHC genes, this effect was replicated in
numerous vertebrate taxa (81). Results of several studies indicate
that in general humans too prefer the odour of MHC different
individuals (82,83). This pattern is, however, reversed in women
using hormonal contraception (84,85), which might have significant consequences on relationship quality and frequency of
break-up (86). It was recently found that couples who met when
the female partner was using hormonal contraception show lower
sexual satisfaction; on the other hand, they report higher level of
overall relationship satisfaction (87). Furthermore, there is ongoing debate on what level of dissimilarity we should expect as
mating with highly dissimilar individuals may suffer from
outbreeding effect, that is, disruption of locally selected gene
complexes (88).
Perspectives: ‘follow your nose!’
We have outlined that human skin is an emitter of olfactory compounds that have the capability to direct our behaviour, consciously or unconsciously. In addition, physicians formerly used
olfactory information for diagnosis. Unfortunately, in today′s hightech medicine, this knowledge seems to have vanished. Among
physicians of different medical specialties, the dermatologist is the
one who approaches the patients closest. In this context, the nose
can still provide valuable information in respect to disease, emotion, age and diet. Furthermore, there is accumulating evidence
that odours from skin glands exert physiological and behavioural
effects. The original definition of a pheromone implies a stereotypical stimulus-response reaction, as known from many insects. In
contrast, the effects in humans seem to be more complex. In the
majority of cases, the reaction towards an odour is dependent on
individual history and actual motivation and, therefore, hardly ever
stereotypical. Furthermore, it is an open question what social and
biological impact the increasing personal hygiene measures typical
for modern societies will have on human life. Could it be that
olfaction in humans is just an aesthetic sense? In most mammals,
657
Kippenberger et al.
Functional receptor genes for
Odorants
Pheromones
VNO –/(?)
VNO +
~300–350
0–5
~850
n.a.
~1100
8
~1000–1200
~270
Figure 1. Evolution of odour and pheromone receptors in mammals. Mouse, dogs
and new-world monkeys have the highest repertoire of functional genes for odorant
receptors. Interestingly, in dogs, intact pheromone receptor genes are decimated.
The red asterisk marks the development of trichromatic colour vision typical for
hominoidea, a superfamily including humans and old-world monkeys such as
chimpanzees, gorillas, orangutans and gibbons. It seems that this evolutionary step
is correlated with pseudogenization of many odorant and pheromone receptor
genes. Moreover, the loss of a functional vomeronasal organ in this superfamily
seems likely. Modified from Rouquier and Giorgi (89). n.a., not available.
odours are perceived by two distinct organs within the nasal cavity,
namely the main olfactory epithelium (MOE), primary responsible
for the perception of odours, and the vomeronasal organ (VNO),
mainly specialized on pheromone-driven effects (89). The VNO
binds volatile and non-volatile chemicals and transmits their signal
to areas of the limbic system (89). Interestingly, recent findings
describe exceptions from the functional separation between VNO
and MOE by detecting pheromone receptors also in the MOE and
vice versa vomeronasal responses to non-pheromonal stimuli
(90,91). In this light, the probable absence of a functional VNO in
adult humans (92) does not necessarily exclude communication via
pheromones. However, it seems that olfactory communication in
humans plays not that essential role as in most other mammals
(see Fig. 1). Of note, recent studies add a new aspect on olfaction
by showing the extra-nasal expression of olfactory receptors. In
particular, functional olfactory receptors are expressed in human
gastrointestinal cells (93), sperm (94) and prostate cells (95). These
amazing findings amend the concept of olfaction. In this context,
it would be intriguing to investigate whether those receptors are
also functionally expressed in human skin.
Acknowledgements
We are grateful to Dr. Adrian Sewell and Jindra Havlı́čková for critically
reading the manuscript. JH is supported by the Grant Agency of Czech
Republic (GACR P407/10/1303) and Charles University Research Centre
(UNCE 204004). All of the authors took part in writing the manuscript
and revising it for final publication.
Conflict of Interest
The authors have declared no conflicting interests.
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