British Journal of Dermatology (1975) 93, .

477
Review
Dispersal of skin microorganisms'
Studies on the dispersal of skin microorganisms can be considered under three headings: investiga-
tions ofthe skin surface and ofthe mechanism of desquamation; hospital or industry based studies
relating to the importance of dispersal; studies aimed at understanding and controlling dispersal.
Skin as a source of organisms
The average human has a skin area of about 175 m^ divided approximately as follows: legs 18%
each, trunk 37%, arms 9% each and head 9%; specialized areas such as the perineum and axillae
account for less than 2% of the total skin area. The skin scales which compose the surface are about
30 X 30 X 3-5 |(m and consequently some 10 are needed to complete the skin surface. Females
have larger scales on average than do males (Plewig, 1970). A complete layer of cells is lost and
replaced on average about every 4 days (Halprin, 1972; Jansen, Hojyo-Tomoko & Kligman, 1974),
hence we all disseminate more than 10^ particles of skin every day. Although clearly bathing or
showering will remove very many scales by mechanical means, Sciple, Riemensnider & Schleyer
(1967) found that natural walking movements released about io* scales per minute. Scales are also
released even when standing naked, presumably because the flakes tend to curl up and become de-
tached when dried on one side only. They are then carried up in the airstream so elegantly demon-
strated by Lewis et al. (1969). Unpublished studies have shown that about 10 mg of skin is deposited
in the clothing in 2 hours.
Microbial skin colonizers are more numerous in some areas than others, for example the head and
thorax carry more microbes than the limbs; males are more heavily colonized with aerobes than are
females, though anaerobes appear to be more equally distributed between the sexes (Table i). A
further complicating factor, however, is that the microorganisms are not spread out equally over their
habitat but live in discrete microcolonies which may be small, ofthe order of 10^ cells, or large, ofthe
order of 10' viable cells. These colonies may be relatively far apart on the skin and this accounts for
the fact that only about 10% of squames carry viable microorganisms (Noble & Davies, 1965).
In disease, especially eczema, psoriasis and pityriasis rosea, the skin may be densely colonized by
Staphylococcus aureus and/or Streptococcus pyogenes. These organisms are then dispersed on skin
scales and such persons may contaminate their environment with these pathogens (Noble & Davies,
1965; Selwyn & Chalmers, 1965; Noble, 1971). Any organism found on the skin surface wi'l be dis-
persed including fluorescent corynebacteria (Somerville-Millar, personal communication), fungi
(Clayton & Noble, 1963; Noble, Lidwell & Kingston, 1963) and presumably viruses. There is some
evidence that smaller skin particles may be involved in dispersal by dermatology patients despite the
large fragments of desquamated skin which are a feature of some skin diseases, though it is not clear
whether this is a reflection ofthe disease process or ofthe greater degree of colonization ofthe skin.
Some individuals may be a potent source of organisms, such as the psoriatic anaesthetist recorded by
Payne (1967) and the eczematous porter (Ayliffe & Collins, 1967). It must be remembered, however,
* Paper based on that presented at the Nordic Association for Contamination Control, Gothenburg, 2-4
April 1975.
477
478 Review
TABLE I. Geometric mean count per square centimetre of skin surface
in eleven normal healthy males and eleven normal healthy females
Site
Forehead
Sternum
Subclavicular area
Centre back
Shoulder
Deltoid area
Forearm
Palm
Lower axilla
Lumbar area
Periumbilical area
Thigh upper front
Thigh lower front
Thigh back
Shin
Calf
Dorsum of foot
Sole
Aerobic
Males
2075
2125
350
450
128
118
250
98
500
300
850
325
350
325
190
173
80
22750
flora
Females
1225
165
130
155
48
65
35
155
92
33
175
140
67
82
77
2 0
1 2 2
675
Anaerobic flora
Males
8000
50000
18500
67500
1025
57
9
33
14
178
55
9
14
4
7
2
3
10
Famales
13500
3500
2275
7500
1075
127
13
85
12
142
80
35
16
5
8
5
1 0
4
Based on data summarized in Somerville & Murphy (1973).
that whilst patients with skin disease are frequently important sources of pathogenic microorganisms,
many dispersers have been discovered who have no clinically apparent epidermal abnormality.
The hair acts as a mechanical sampler of the environment and several studies have recorded the
propensity ofthe hair to carry Staph. aureus and oer pathogens (Summers, Lynch & Black, 1965;
Black, 1966; Noble, 1966; Black, Bannerman & Black, 1974). Opinion is divided as to the role ofthe
hair in dispersal.
Definition of a 'disperser^
In a study of dispersal in hospital wards Noble (1962) defined as a disperser of Staph. aureus a patient
who contributed more than 0-2 Staph. aureus particles per cubic foot (6/m^) to the air of a ward
housing many patients. Since the mean air-count of all organisms was of the order of 27 viable
particles per cubic foot (800/m^), this figure was equivalent to about 1% of the total flora. Noble &
Davies (1965) later adopted a less stringent definition requiring a 'disperser of Staph. aureus' to
disseminate this organism as more than 1% of his total flora whilst undressing in a cubicle of about 100
cubic foot (2-8 m^) capacity. Bethune et al. (1965) defined as a disperser of Staph. aureus one who
disseminated more than 10 Staph. aureus particles into the air of a 100 cubic foot chamber during
exercise; Blowers, Hill & Howell (1973) later amended this to 4 Staph. aureus particles/m^. This is
clearly of the same order as the definition proposed by Noble & Davies.
Dispersal is, of course, a very variable event. Even in studies ofthe normal fiora, where presence or
absence of a specific organism does not influence the result, the standard deviation of the mean air
count during undressing is of the order of 50% (Table 2).
Review 479
TABLE 2. Dispersal of organisms by various individuals. Throughout
each investigations each individual used the same hygienic regimen
Individual
I
2
3
4
5
6
7
8
9
1 0
I I
Sex
F
F
F
F
M
F
M
F
F
M
M
No. of
samples
9
6
7
6
10
1 0
2 0
9
9
6
7
Mean
air count
during
undressing
825
669
998
886
657
2315
1320
847
1720
1316
582
S.D.
216
240
375
340
270
1050
645
450
955
830
535
S.D. as %
of mean
26
36
38
38
41
45
49
53
56
63
92
Based on material summarized in Wilson (1970).
Dispersal as a hazard
Early studies of dispersal include those of deForest & Kerr (1945) who reported a case of eczema as a
source of streptococci; Loosli and his colleagues (1950) who identified 'skin dispersers' as sources of
streptococci in wards for neonates; and those of Hare and his co-workers who firmly implicated
patients with eczema and mycosis fungoides as potent sources of airborne microorganisms (Hare &
Ridley, 1958; Hare & Cooke, 1961). Duguid& Wallace (1948) had already identified dust from clothing
as a means by which organisms became airborne and distributed about the environment.
Studies of staphylococcal cross-infection in hospital wards gave a boost to studies of dispersal and
acquisition. Staph. aureus was shown to be spread round hospital wards, appearing in the noses and
less frequently in the lesions of surgical patients (Williams et al., 1962; Noble, 1962). Debate on the
nature of the 'fibre nuclei' believed to be responsible for dissemination from bedclothes led to the
rediscovery of skin scales as the raft on which microorganisms became airborne (Davies & Noble,
1962). A raft of some nature was predictable from the aerodynamic behaviour of the particles.
Although on average only 4 viable Staph. aureus cells appeared to make up each airborne particle
(Lidwell, Noble & Dolphin, 1959) the particles were shown to be about 14 ^m in equivalent diameter;
a particle big enough to be composed of some hundreds of cocci (Noble, Lidwell & Kingston, 1963). It
should perhaps be emphasized that, for reasons of mathematical convenience, airborne particles are
best considered as spheres having unit density. Thus on average the 30 x 30 x 3-5 ^m flakes behave in
the same fashion as spheres of 14 //m diameter.
Although the mean is around 14 /im equivalent diameter there is a considerable range in size ofthe
individual particles. Table 3 shows the range in sizes derived from data summarized in Noble &
Davies (1965). The range is broadly comparable with that reported by Clayton & Noble (1963) for
particles bearing fungi obtained during examination of patients in a mycology clinic. The median
diameters are greater than those obtained for skin scales alone (8 /im, Davies & Noble, 1962); this is
presumably a reflection of the greater chance that larger particles will bear bacteria. May & Pomeroy
(1973) published size distribution data which showed that 45% of particles from males and 28% of
particles from females were too large to remain airborne (over 60 jum equivalent diameter). When air-
480 Review
TABLE 3. Size distribution of airborne particles in dispersal experiments based on data sum-
marized in Noble & Davies (1965)
Population
Normal flora
Normal Normal Adult Infant
adult adult surgical eczema
males females patients patients
16746 263774 28940
Staph. aureus
Adult Infant
surgical eczema
patients patients
10048 18213
No. of 12 12 21 8
individuals
Total colony 76614
forming units
contributing
Cumulative %
of particles greater
than 18 2 /xm 43 39 28 30
96 //m 79 75 65 36
42 fim 95 94 89 95
Median equivalent 17 16 13 14
diameter (//m)
34
72
90
145
II
57
86
borne particles only were considered, about 27% were over 20 ^m and 11% less than 5 fim, values
equivalent to those shown in Table 3.
That these airborne particles were in fact skin scales was necessarily an inference for there is no
specific stain for keratin; yet the particles were composed of protein and contained some fat, they
bore human blood group substances (demonstrated by the Coombs' technique (Coombs, Bedford &
Rouillard, 1956)), they carried human skin organisms and finally they looked like skin scales (Davies &
Noble, 1962). Little else could be imagined which would fit these criteria. The way was then open for
studies on methods of preventing dispersal. The principal lines of attack were the use of antibacterial
agents and of squame-proof clothing.
Dispersal from hair. Dineen & Drusin (1973) reported that dispersal of Staph. aureus from the scalp
of two individuals in an operating theatre resulted in post-operative wound infection. One ofthe two
individuals had frank scalp lesions which drained pus prior to the epidemic of infection. A more subtle
hazard is presented by the fashion for wearing beards and has stimulated much editorial comment but
httle investigation. Barbeito, Mathews & Taylor (1967) found that nuzzling into an infected beard
could transmit infection to guinea-pigs. However, Dr A.G.M.Huysmans-Evers (personal communica-
tion) has found that thirteen individuals of a total of eighty-four carried Staph. aureus on the beard and
that seven of these thirteen dispersed this organism and were thus a potential hazard.
Reduction of dispersal. Antibacterial agents such as hexachlorophane and trichlorocarbanilide
(TCC) when used regularly in a soap formulation have a statistically significant effect in reducing the
skin flora (Solberg, 1965; Speers et al., 1966; Wilson, 1970). There has, however, been a move away
from the use of these compounds following the reports of brain damage resulting from absorption of
hexachlorophane. Antibiotic treatment of carrier sites also reduces the dispersal of pathogens (Varga &
White, 1961; Solberg, 1965). Redesign of clothing has been pursued with more vigour. Normal
Review 481
fabrics have very large pores between the woven threads and these pores permit the easy passage of
skin scales. 'Ventile' fabric, however, has a very close weave which does not permit the passage of
scales and so reduces dispersal. Redesign of operating theatre clothing itself, with less loose openings,
also reduces the bacterial load disseminated during operations (Bernard et al, 1965; Bethune et al,
1965; Charnley & Eftekhar, 1969).
It is clear from the work of May & Pomeroy (1973), Hill, Howell & Blowers (1974) and Mitchell &
Gamble (1974) that clothing that specifically occludes the perineum significantly reduces dispersal.
Yet, as Ayliffe, Babb & Collins (1974) pointed out, this is of value only when the perineum is the
prime source of organisms. Where nasal carriers are concerned (White, 1961; Solberg, 1965) occlusive
clothing is of little value and Ayliffe and his colleagues suggested that it be reserved for high risk
operations, such as hip replacement (Charnley, 1973).
The hazard in dispersal of Staph. aureus or any other potential pathogen lies in the chance that the
organism will find its way into an otherwise sterile field. In industry Sykes (1970) has pointed out that
a room can be designed and maintained 'virtually sterile' tintil it is occupied by himians; such condi-
tions are required for sterile filling of injectable materials. Favero et al. (1966) have reported essentially
similar studies whilst Behagel & Berg (1973) reported on the difficulty of maintaining staphylococcal
cultures free from the risk of contamination by phage derived from strains carried by personnel. In a
hospital situation the gravest risk is in the operating theatre (Payne, 1967; Ayliffe & Collins, 1967;
Charnley, 1973), but there is also a general risk in the excessive dispersal of organisms into the air of
wards (Hamburger, Green & Hamburger, 1945; Noble, 1962; Schaffner et al, 1969). In operating
theatre outbreaks it is fairly easy to document and ascribe infection to one individual; in the instance
quoted by Payne (1967) there were four deaths amongst the thirty-three patients involved and the
source was an anaesthetist with psoriasis. It is less easy to be specific in ward outbreaks though Lid-
well & Brock (1973) have demonstrated the relationship between dispersal and nasal acquisition.
Intrinsic interest in dispersal
Although in total the process of dispersal is clearly a mechanical one, there have been a number of
curious facets which created an interest in dispersal as a research topic.
In the studies carried out by Shooter and Blowers and their colleagues it was foimd that, following
showerbathing, there was often an increase in the dispersal of non-pathogenic organisms, despite the
fact that showering clearly removed thousands of organisms from the skin. This may best be ex-
plained by reference to the microcolonies of bacteria on the skin surface. During washing, many of the
bacteria in the colonies are removed mechanically but others are spread out over the skin surface thus
contaminating more scales than previously. Sebtmi is also removed during washing which may leave
the skin temporarily more susceptible to desiccation so that scales may dry, curl up and become free
more readily than when sebum is abundant. After a short periodas little as 2 hoursthe skin
returns to normal. This is illustrated in the work of Holt (1971) who found that the average micro-
colony size decreased following washing or bathing, as did the count of total bacteria, but that tem-
porarily the contact count, which measures the number of independent viable units, increased. This
increase in dispersal of normal fiora following showering led to suggestions that surgeons abandon the
traditional shower before operation, despite the demonstration by Cleton, van der Mark & van Toorn
(1968) that contaminant pathogenic organisms, which would include those acquired during ward
rounds, etc. are all removed by the shower.
Another curious observation was that normal healthy males dispersed more than did females,
especially when clad in 'street' clothing. The sex difference was reduced when the same clothing or no
clothing was worn but it persisted (Table 4). Although Noble & Davies (1965) could not ascribe
differences in dispersal to differences in size between males and females, a re-examination of their
482 Review
TABLE 4. Sex ratio of total flora dispersal under different degree of clothing. All air samples in a cubicle
Method of
measuring
dispersal
tJndressing
Walking on spot
Exercise
Exercise, rub
skin or clothing
Exercise
tJndressing
Undressing
Clothing
Street
Cotton pyjamas
Street
Nil before shower
Nil after shower
Street
Swim suit
Street
Nil
Street
Nil
Street
Street
No. of
samples
42
42
46
2 0
46
1 0
10
28
28
16
16
54
72
No. of
individuals
42
42
1 0
1 0
1 0
1 0
1 0
28
28
9
9
9
72
Ratio
male/female
41 \
1 4 /
3-31
2-0 y
4-71
ro/
13I
5 2 /
4 9 /
I 22
3-6
Authors
Noble & Davies (t965)
Speers et al. (1965)
Doig (1972)
May & Pomeroy (1973)
Ballard & Lidwell
(personal communication)
Wilson (personal communi-
cation)
Noble, et al.
(in preparation)
data in the light of Plewig's (1970) report that females have larger scales thati males is ititeresting. It
can be calculated that, on the basis of differences in squame size, males ought to disperse about 1-25
times as many squames as do females. The skin areas of the people studied by Noble & Davies were
available and, since the males were on average larger, a further factor of i-i6 might be added. Males
ought then to disperse 1-45 times as many scales as do females; the sex ratio for dispersal of scales found
by Noble & Davies was 1-34. There is, however, a further factor to be taken into account when we
discuss dispersal of bacteria. It is that males are more heavily colonized with bacteria than are females
(Table i). In,a study of surgical persotmel (Noble et al, in preparation) it was found that, although
males dispersed about 3-5 times as many bacteria as do females, the sex difference disappeared if
allowance was made for the denser colonization of males.
Perhaps more striking is the observation that very few healthy young women disperse Staph.
aureus. The most extensive studies have been those of Hill, Howell & Blowers (1974) who have de-
tected forty-five dispersers of Staph. aureus amongst 389 men but only eight amongst 613 women. It
seemed possible that this was under hormonal influence but examination of 100 post-menopausal
women has also failed to reveal more than five dispersers (Mitchell & Gamble, 1974).
Others, however (Solberg, 1965; Oud, 1969; Solberg, Bruun & Boe, 1972), have found female dis-
persers of Staph. aureus though they are much less active than males. On a rank order basis males
significantly outrank females. This male predominance does not extend to patients, however; studies
on airborne staphylococci have failed to reveal differences between males and females in the degree
of dissemination in hospital wards (Lidwell & Brock, 1973). Some studies help to throw light on this
phenomenon. The classic work of Solberg (1965) showed that the degree of dispersal of Staph. aureus
was directly related to the degree of contamination of the skin with this organism. Blowers' investiga-
tions had previously shown that, in experiments where persons in operating theatre clothing exercised
in a cubicle, dispersal was mainly from below the waist. Recent studies in the Netherlands (Noble
et al, in preparation) showed that, in experiments in which undressing was the means of dispersal, the
Review 483
correlation (analysed by a forward stepwise regression analysis) between dispersal and body site was
most significant for the abdomen and thighs in males and for the shin in the females (perhaps due to
the 'cheese-grater' effect of tights and stockings described by Mitchell & Gamble, 1974). If this
difference is found to be true for studies of exercising rather than imdressing, the predominance of
males in dispersing Staph. aureus might be ascribed simply to greater contamination of the thighs than
the shins with perineal organisms.
There is still much that remains to be discovered in relation to dispersal. Why are males more
heavily colonized with skin bacteria than are females ? Why do some individuals without skin disease
carry Staph. aureus on the skin for shortor longperiods ? Can differences in clothing accoimt for
differences in dispersal pattern, and finally can dispersal of potential pathogens be prevented without
recourse to hot, perhaps uncomfortable, operating theatre clothing and without the application of
apparently harmful skin degerming compounds ?
Department of Bacteriology, W.C.NOBLE
St John's Hospital for Diseases
of the Skin,
Homerton Grove,
London E9 6BX
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