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Review Article
Abstract This review describes the role of pH in cutaneous structure and function. We first describe the molecules that contribute to the acidity or alkalinity of the skin. Next, differences in cutaneous pH among species,
among individuals of the same species and within individuals are described. The potential functions of cutaneous
pH in normal and diseased skin are analysed. For example, cutaneous pH has a role in the selection and maintenance of the normal cutaneous microbiota. In addition, cutaneous acidity may protect the skin against infection
by microbes. Finally, there is evidence that a cutaneous pH gradient activates pH-dependent enzymes involved
in the process of keratinization.
Keywords: animal, comparative, cutaneous, human, review, skin pH
INTRODUCTION
The role cutaneous pH plays in the barrier function of
the skin has been a matter of debate for over a century.
Human skin pH is relatively acidic (4.04.9) compared
with the skin of many animal species (Table 1).15 Most
investigators believe that the acidity of human skin
serves to protect it from invasion by micro-organisms.6,7
More recent findings show that pH also influences
the permeability barrier of the skin and the normal
keratinization process.8,9 Information regarding
cutaneous pH in animals is sparse. The following is a
Table 1. Includes the average of reported cutaneous pH values
for several mammalian species. 4,6,20,24,25,2830,43 48 pH levels were
measured using different techniques, and may not be directly
comparable
Mammalian species
Average reported pH
Human
Guinea pig
Goat
Pig
Horse
Cat
Monkey
Rat
Cattle
Rabbit
Dog
Sheep
4.8
5.5
5.9
6.3
6.3
6.4
6.4
6.5
6.7
6.7
7.4
8.1
ORIGINS OF CUTANEOUS PH
The symbol pH is used to indicate the potzen (German
for power) or concentration of hydrogen ion (H+) in a
solution. Specifically, pH represents the logarithmic
reciprocal of the H+ concentration (pH = log 1/H+).7,10
A pH of 7.0 is considered neutral. A pH of < 7.0 is
considered acidic, whereas a pH > 7.0 is considered
alkaline.11 Therefore, as the pH number increases, the
concentration of H+ (acidity) decreases. It is important
to remember that pH is measured on a logarithmic
scale with 10 as its base, which means that each change
of 1 pH unit corresponds to a 10-fold change in H+
concentration. The difference between a pH of 5.0 and
5.3 (0.5 105 gram ion per litre) is greater than the
difference between a pH of 7.0 and 7.3 (0.5 107 gram
ion per litre).10 In addition, because of the logarithmic
scale, the H+ concentration at a pH of 5.0, is twice that
at a pH of 5.3.10
The pH of the skin results from a combination of
factors derived from the epidermal cells and glands
(sebaceous, apocrine, eccrine). This buffering system of
acidic and alkaline molecules maintains the pH of the skin
within a normal range. Most information regarding
the origins of cutaneous pH is derived from studies in
people and rodents.
The original acid mantle theory proposed that a
surface film of molecules was responsible for cutaneous
acidity. Two methods have been used to show that the
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294
Cutaneous pH
sweating. These two types of sweat, and their respective
effects on the cutaneous pH, differ. Normal eccrine sweat
is acidic (4.56.0) and the skin becomes more acidic as
the sweat evaporates (normally ammonia evaporates
quickly).41 As the rate of eccrine sweat increases, the
concentrations of ammonia, pyruvic acid and lactate
decrease, and the pH increases.23,41 Thermal apocrine
sweat has a higher pH than eccrine sweat, and the skin
pH becomes higher as it evaporates.16,26,30
Abe et al.42 demonstrated a seasonal effect on cutaneous
pH. Measurements were taken in a nonair-conditioned
room, in which the temperature and relative humidity
was highest in July (27.5C, 70.5%) and lowest in January
(15.1C, 35.1%). There was an inverse relationship
between skin surface pH and environmental temperature the pH was the lowest in July. They proposed that
this change was due to an overall increase in eccrine
sweat production.
Yosipovitch et al.29 determined that circadian rhythms
in human skin pH are present on the forearm and shin,
but not on the forehead or back. In most of the people
studied, maximum pH levels occurred in the afternoon
(14.0016.00), and lowest levels occurred in the evening
(20.00). These results conflict with those of Ehlers
et al.38 who evaluated forearm pH from 08.00 to 15.00,
and showed a decrease in pH throughout the day, with
lowest values occurring at 15.00. The relevance of these
findings are uncertain. Yosipovitch et al.29 speculated
that the pH changes reflect circadian variation in stratum
corneum enzyme activities, but to date there are no
reports on the rhythmicity of enzyme function in the
epidermis. It is possible that circadian variations are
influenced by other factors, such as climate, physical
activity, age or previous soap use.
Canine
Canine skin pH differs from human skin, and tends to
be the highest of the mammalian species.25 Reports of
normal canine pH have ranged from 4.84 to 9.95.25,4345
Although many investigators indicate that the most
common pH range for canine skin is 5.57.2, it may
actually be higher. In a study by Ruedisueli et al.45 the
mean pH on the flanks of dogs was 7.48. The authors
have also observed a higher cutaneous pH range on the
dorsal thoracolumbar area of dogs (6.49.1).46
Previous researchers have not identified a significant
association between gender and skin pH in dogs43 but
Ruedisueli et al.45 reported that the cutaneous pH of
males was higher than females. In addition, the skin of
neutered female dogs was higher than that of intact
females.45 There is a significant difference in mean pH
related to dog breeds: Labrador Retriever (7.13),
Miniature Schnauzer (7.25), Springer Spaniel (6.65),
and Yorkshire Terrier (7.71) dogs.45 As in people, the
pH levels from different anatomic sites in dogs are
significantly different.45
Meyer et al.43 reported that excitement in dogs can
lead to elevations in cutaneous pH levels. The pH range
in unexcited dogs was 4.847.70, whereas that in excited
dogs was 6.609.95. They proposed that the elevation
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296
FUNCTIONS OF CUTANEOUS PH
As stated previously, the role cutaneous pH plays in the
epidermal barrier has not been fully defined. Functions
of the epidermis can be accomplished through several
different mechanisms. For example, protection from
invasion by micro-organisms is controlled by microbial
desiccation, competition with resident microbiota, and
an acidic pH. It can be difficult to evaluate these effects
independent of one another.
Antimicrobial
Since the realization that the surface of human skin
was acidic, investigators have theorized that this acidity served to protect the skin from bacterial and yeast
infections.6,7 In general, higher bacterial counts are
retrieved from skin with alkaline pH levels.49 In addition, when gram-negative bacteria are placed onto
alkaline skin, they disappear more slowly than they do
on acidic skin.49 Although this may not be the primary
defence mechanism against cutaneous pathogens, the
relatively alkaline pH of canine skin may contribute
to the increased frequency of skin infections in dogs
relative to people and other animal species.50 There are
other possible reasons for the increased incidence of
staphylococcal pyoderma in the dog. Compared with
other species, electron microscopy of the canine
epidermis reveals a relatively thin and compact stratum
corneum, less intercellular lipid, and the lack of a protective lipid plug around the hair follicle infundibulum.51,52 Second, dogs may have a higher level of
cutaneous carriage of bacteria than other species, such
as cats, who have a low occurrence of skin infections.
Krogh and Kristensen53 found that 50% of skin swabs
from 10 normal cats were sterile compared with 20% in
dogs.53 Lastly, because Staphylococcus intermedius is
not a highly virulent organism, disruption of the host
immune defences and immune response are considered
important determinants as to whether infection will
2002 Blackwell Science Ltd, Veterinary Dermatology, 13, 293 300
occur in a particular animal.54 Disorders that predispose dogs to bacterial pyoderma are numerous, and
include hypersensitivity disorders, poor grooming habits,
immune suppression and endocrinopathies.
In vitro and in vivo studies have proven that cutaneous pH can affect the growth of skin microbiota. In
general, a pH of less than 4.0 or 5.0 prevents microbial
growth.24 Although most cutaneous biota can survive
at all of the pH levels found on the skin, small changes
may create an advantage or disadvantage for particular
organisms. An example of this was demonstrated by
Korting et al.55 when they cultured Staphylococcus
epidermidis, Staphylococcus aureus and Propionibacterium
acnes at pH levels ranging from 5.5 to 8.5 (0.5 pH
increments) in vitro. They found that neither of the
staphylococcal species exhibited a difference in growth
rate between pH values of 5.57.0. In contrast, P. acnes
did not grow at a pH of 5.5, and exhibited optimal
growth at pH levels of 6.07.0. Thus, small shifts within
the acidic range, would be expected to affect the growth
of P. acnes more than that of Staphylococci. These
results were supported by several in vivo studies.2,56,57
In one study, the patients washed their forehead and
forearm with synthetic detergents of either pH 5.5 or
8.5.2 Both detergents were identical, except NaOH was
added to adjust the pH. There was a significant correlation between the skin pH and the pH of the product
(the skin was more alkaline with the pH 8.5 synthetic
detergent). Additionally, cutaneous counts of Propionibacterium sp. were significantly higher when the
alkaline cleanser was used. Although the numbers of
cutaneous Staphylococcus sp. increased slightly with
the alkaline preparation, the amount was not significant. A similar study, evaluating products with pH
values of 5.5 and 7.0 yielded similar conclusions.56
These investigations were interesting for several reasons. First, they demonstrated that cutaneous pH plays
a role in controlling bacterial populations on the skin
surface. The extent of the effect of cutaneous pH on the
skin microbiota of other mammals has yet to be determined. It is possible that in mammals with alkaline
skin pH levels (e.g. dogs), the pH may not play as much
of a role in controlling cutaneous bacteria and yeast
populations as it does in those with acidic skin (e.g.
humans). Second, they showed that the growth of
various species of micro-organisms is affected differently
by alterations of pH. In humans, whose normal skin
pH ranges from 3.0 to 6.5, the carriage of staphylococal species was not significantly altered by pH changes
of 5.57.0. It is possible that more extreme changes
in cutaneous pH are needed to alter the carriage of
staphylococcal species. The cutaneous pH of dogs is
higher (4.849.95) than that of people, so the cutaneous pH of dogs would probably need to be decreased
significantly to affect the growth of S. intermedius.
Third, they proved that topical products could change
both the pH and the microbiota of the skin. Unfortunately, similar studies have not been performed in dogs.
In a study evaluating the effects of four acidifying
sprays (pH 2.23.0), vinegar (pH 2.7) and water
Cutaneous pH
(pH 5.7) on canine cutaneous pH, the acidifying sprays
led to a decrease in skin pH from a mean of 7.55 (range
6.39.0) to < 6.0 for a mean duration of 5065 h, while
the vinegar did so for 12 h.46 This study demonstrated
that canine skin pH can be decreased with the use of
acidifying topical products, but did not evaluate the
effect that this may have on cutaneous microbiota.
More investigations are needed to determine if changes
in canine skin pH will lead to alterations in cutaneous
carriage of bacteria and yeast. Concern has been
expressed that the low pH of topical acidifying products may cause cutaneous irritation. Although many
shampoos and conditioners for people are manufactured
to be pH-balanced, studies evaluating the irritancy of
acidifying topical products are conflicting. For the
most part, investigators have shown that the ingredients
of the topical product are more likely to be the cause of
irritation than the pH of the product.5862
In addition to affecting the multiplication of microbes,
cutaneous pH may also alter the virulence of an organism or the susceptibility of the host. An example of this
was demonstrated by Runeman et al.63 when they
experimentally induced Candidal dermatitis under
different pH conditions. They applied Candida albicans
to occlusive patches with pH buffers of 6.0 or 4.5, and
attached these patches onto the forearms of 15 women.
Twenty-four hours after occlusion, the appearance of
skin lesions was significantly (P < 0.0001) more severe
at the control site (pH 6.0) than at the acidic site
(pH 4.5). Despite differences in the visual assessment
of cutaneous lesions, cultures acquired with a scrub
technique showed no significant difference (P = 0.64)
in the amount (cfu/cm2) of C. albicans among the lesions.
One explanation for these findings is that alkaline pH
levels favour the mycelial form of C. albicans, which is
more pathogenic than the yeast form. The authors
concluded that although a relatively alkaline skin pH
does not affect overall cutaneous carriage of yeast, it
does predispose the skin to infection by C. albicans.
Maintenance of normal cutaneous microbiota
The species density of cutaneous microbiota differs at
various anatomic locations. The pH of the skin may
play a role in selecting the resident bacteria and yeast
populations. In vitro, Brevibacterium epidermidis grew
rapidly at pH levels of 5.58.5, but no growth occurred
at a pH of 5.0.1 This organism is primarily located in
the axillae of people, where the cutaneous pH tends to
be neutral to alkaline. Although other factors (skin
temperature, humidity, glandular production) likely
contribute to the maintenance of bacterial and yeast
populations, pH probably has a role.
Keratinization and desquamation
The processes of keratinization and desquamation are
complex, involving changes in keratins, lipids and
enzyme functions. In the past 20 years, investigators
have established that the pH gradient found between
the upper granular layer and the stratum corneum is not
just an innocent bystander. This gradient is thought to
297
DISEASED SKIN
The importance of pH is also demonstrated in disease
states. Some diseases are associated with an increase in
2002 Blackwell Science Ltd, Veterinary Dermatology, 13, 293300
298
CONCLUSION
In conclusion, it is clear that cutaneous pH values
differ among animals and people. Although debate still
exists over the significance of cutaneous pH, there is
evidence for its roles in the normal keratinization
process and barrier functions of the skin. In addition,
alterations in cutaneous pH may occur as a result of a
cutaneous disorder, or may predispose the skin to disease. Future studies should help further define the role
of cutaneous pH in animals and people.
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Rsum Cet article dcrit le rle du pH dans les structures et les fonctions cutanes. Les molcules contribuant
lacidit ou lalcalinit cutane sont dabord dcrites. Puis les diffrences de pH cutan en fonction des espces,
des individus et pour chaque individu sont rapportes. Les fonctions possibles du pH cutan sont analyses
pour la peau normale et pour les dermatoses. Par exemple, le pH cutan prsente un rle de slection et de
maintenance de la flore cutane normale. En outr, lacidit cutane pourrait protger la peau contre les
infections par des microbes. Enfin, un gradient de pH cutan active des enzymes dpendant du pH, impliques
dans le processus de keratinisation.
Resumen Esta revisin describe el papel del pH en la estructura y funcin cutnea. Primero se describen las
molculas que contribuyen a la acidez o alcalinidad de la piel. Despus, se describen las diferencias en el pH
cutneo entre especies, entre individuos de la misma especie y entre individuos. Se analizan las funciones
potenciales del pH cutneo en piel normal y enferma. Por ejemplo, el pH cutneo tiene un papel en la seleccin
y mantenimiento de la flora cutnea normal. Adems, la acidez cutnea puede proteger la piel contra infecciones
microbianas. Finalmente, est probado que un gradiente del pH cutneo activa los enzimas pH-dependientes
implicados en el proceso de queratinizacin.
Zusammenfassung Diese bersicht beschreibt die Rolle des kutanen pH fr die Struktur und Funktion der
Haut. Zuerst werden die Molekle beschrieben, die zum Suregrad oder zur Alkalitt der Haut beitragen. Dann
werden Unterschiede im kutanen pH zwischen Spezies, zwischen Individuen derselben Spezies und innerhalb
einzelner Individuen beschrieben. Die mglichen Funktionen des kutanen pH in normaler und erkrankter Haut
werden analysiert. Zum Beispiel spielt der kutane pH eine Rolle in der Auswahl und Erhaltung der normalen
kutanen Mikroflora. Zustzlich schtzt der kutane Suregrad die Haut mglicherweise gegen mikrobielle
Infektionen. Und schliesslich gibt es Hinweise darauf, dass der kutane pH Gradient am Keratinisierungsprozess
beteiligte pH-abhngige Enzyme aktiviert.
2002 Blackwell Science Ltd, Veterinary Dermatology, 13, 293 300