British Journal of Dermatology (1975) 93, .477Review

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 studiesrelating to the importance of dispersal; studies aimed at understanding and controlling dispersal.

Skin as a source of organismsThe 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 axillaeaccount for less than 2% of the total skin area. The skin scales which compose the surface are about30 X 30 X 3-5 |(m and consequently some 10 are needed to complete the skin surface. Femaleshave larger scales on average than do males (Plewig, 1970). A complete layer of cells is lost andreplaced 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 orshowering 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 alsoreleased 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 Unpublished studies have shown that about 10 mg of skin is depositedin the clothing in 2 hours.

Microbial skin colonizers are more numerous in some areas than others, for example the head andthorax carry more microbes than the limbs; males are more heavily colonized with aerobes than arefemales, though anaerobes appear to be more equally distributed between the sexes (Table i). Afurther complicating factor, however, is that the microorganisms are not spread out equally over theirhabitat but live in discrete microcolonies which may be small, ofthe order of 10^ cells, or large, oftheorder of 10' viable cells. These colonies may be relatively far apart on the skin and this accounts forthe 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 byStaphylococcus aureus and/or Streptococcus pyogenes. These organisms are then dispersed on skinscales 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 someevidence that smaller skin particles may be involved in dispersal by dermatology patients despite thelarge fragments of desquamated skin which are a feature of some skin diseases, though it is not clearwhether 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 byPayne (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, 2-4April 1975.

477

478 ReviewTABLE I. Geometric mean count per square centimetre of skin surface

in eleven normal healthy males and eleven normal healthy females

Site

ForeheadSternumSubclavicular areaCentre backShoulderDeltoid areaForearmPalmLower axillaLumbar areaPeriumbilical areaThigh upper frontThigh lower frontThigh backShinCalfDorsum of footSole

Aerobic

Males

20752125

350450128118250

98500300850325350325190173

8022750

flora

Females

1225165130155486535

1559233

1751406782772 0

1 2 2

675

Anaerobic flora

Males

8000500001850067500

102557

93314

17855

914472

31 0

Famales

135003500227575001075

127138512

142803516585

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 thepropensity 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 ofthehair in dispersal.

Definition of a 'disperser^In a study of dispersal in hospital wards Noble (1962) defined as a disperser of Staph. aureus a patientwho contributed more than 0-2 Staph. aureus particles per cubic foot (6/m^) to the air of a wardhousing many patients. Since the mean air-count of all organisms was of the order of 27 viableparticles 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' todisseminate this organism as more than 1% of his total flora whilst undressing in a cubicle of about 100cubic foot (2-8 m^) capacity. Bethune et al. (1965) defined as a disperser of Staph. aureus one whodisseminated more than 10 Staph. aureus particles into the air of a 100 cubic foot chamber duringexercise; Blowers, Hill & Howell (1973) later amended this to 4 Staph. aureus particles/m^. This isclearly 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 orabsence of a specific organism does not influence the result, the standard deviation of the mean aircount during undressing is of the order of 50% (Table 2).

Review 479TABLE 2. Dispersal of organisms by various individuals. Throughout

each investigations each individual used the same hygienic regimen

Individual

I

2

3456789

1 0I I

Sex

FFFFMFMFFMM

No. ofsamples

9676

1 01 02 0

9967

Meanair count

duringundressing

825669998886657

23151320847

17201316

582

S.D.

216240375340270

1050645450955830535

S.D. as %of mean

2636383841454953566392

Based on material summarized in Wilson (1970).

Dispersal as a hazardEarly studies of dispersal include those of deForest & Kerr (1945) who reported a case of eczema as asource of streptococci; Loosli and his colleagues (1950) who identified 'skin dispersers' as sources ofstreptococci in wards for neonates; and those of Hare and his co-workers who firmly implicatedpatients 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 clothingas 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 andacquisition. Staph. aureus was shown to be spread round hospital wards, appearing in the noses andless frequently in the lesions of surgical patients (Williams et al., 1962; Noble, 1962). Debate on thenature of the 'fibre nuclei' believed to be responsible for dissemination from bedclothes led to therediscovery 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). Itshould perhaps be emphasized that, for reasons of mathematical convenience, airborne particles arebest considered as spheres having unit density. Thus on average the 30 x 30 x 3-5 ^m flakes behave inthe same fashion as spheres of 14 //m diameter.

Although the mean is around 14 /im equivalent diameter there is a considerable range in size oftheindividual 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) forparticles bearing fungi obtained during examination of patients in a mycology clinic. The mediandiameters are greater than those obtained for skin scales alone (8 /im, Davies & Noble, 1962); this ispresumably 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% ofparticles from females were too large to remain airborne (over 60 jum equivalent diameter). When air-

480 ReviewTABLE 3. Size distribution of airborne particles in dispersal experiments based on data sum-

marized in Noble & Davies (1965)

Population

Normal flora

Normal Normal Adult Infantadult adult surgical eczemamales females patients patients

16746 263774 28940

Staph. aureus

Adult Infantsurgical eczemapatients patients

10048 18213

No. of 12 12 21 8individualsTotal colony 76614forming unitscontributingCumulative %of particles greaterthan 18 2 /xm 43 39 28 30

96 //m 79 75 65 3642 fim 95 94 89 95

Median equivalent 17 16 13 14diameter (//m)

347290

145

II5786

borne particles only were considered, about 27% were over 20 ^m and 11% less than 5 fim, valuesequivalent to those shown in Table 3.

That these airborne particles were in fact skin scales was necessarily an inference for there is nospecific stain for keratin; yet the particles were composed of protein and contained some fat, theybore 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 forstudies on methods of preventing dispersal. The principal lines of attack were the use of antibacterialagents and of squame-proof clothing.

Dispersal from hair. Dineen & Drusin (1973) reported that dispersal of Staph. aureus from the scalpof two individuals in an operating theatre resulted in post-operative wound infection. One ofthe twoindividuals had frank scalp lesions which drained pus prior to the epidemic of infection. A more subtlehazard is presented by the fashion for wearing beards and has stimulated much editorial comment buthttle investigation. Barbeito, Mathews & Taylor (1967) found that nuzzling into an infected beardcould 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 andthat 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 theskin flora (Solberg, 1965; Speers et al., 1966; Wilson, 1970). There has, however, been a move awayfrom the use of these compounds following the reports of brain damage resulting from absorption ofhexachlorophane. 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 ofskin scales. 'Ventile' fabric, however, has a very close weave which does not permit the passage ofscales 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 theprime source of organisms. Where nasal carriers are concerned (White, 1961; Solberg, 1965) occlusiveclothing is of little value and Ayliffe and his colleagues suggested that it be reserved for high riskoperations, such as hip replacement (Charnley, 1973).

The hazard in dispersal of Staph. aureus or any other potential pathogen lies in the chance that theorganism will find its way into an otherwise sterile field. In industry Sykes (1970) has pointed out thata 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 essentiallysimilar studies whilst Behagel & Berg (1973) reported on the difficulty of maintaining staphylococcalcultures free from the risk of contamination by phage derived from strains carried by personnel. In ahospital 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 ofwards (Hamburger, Green & Hamburger, 1945; Noble, 1962; Schaffner et al, 1969). In operatingtheatre outbreaks it is fairly easy to document and ascribe infection to one individual; in the instancequoted by Payne (1967) there were four deaths amongst the thirty-three patients involved and thesource 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 dispersalAlthough in total the process of dispersal is clearly a mechanical one, there have been a number ofcurious 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, followingshowerbathing, there was often an increase in the dispersal of non-pathogenic organisms, despite thefact 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 thebacteria in the colonies are removed mechanically but others are spread out over the skin surface thuscontaminating more scales than previously. Sebtmi is also removed during washing which may leavethe skin temporarily more susceptible to desiccation so that scales may dry, curl up and become freemore readily than when sebum is abundant. After a short periodas little as 2 hoursthe skinreturns 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. Thisincrease in dispersal of normal fiora following showering led to suggestions that surgeons abandon thetraditional shower before operation, despite the demonstration by Cleton, van der Mark & van Toorn(1968) that contaminant pathogenic organisms, which would include those acquired during wardrounds, 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 noclothing was worn but it persisted (Table 4). Although Noble & Davies (1965) could not ascribedifferences in dispersal to differences in size between males and females, a re-examination of their

482 ReviewTABLE 4. Sex ratio of total flora dispersal under different degree of clothing. All air samples in a cubicle

Method ofmeasuringdispersal

tJndressing

Walking on spot

Exercise

Exercise, rubskin or clothingExercise

tJndressing

Undressing

Clothing

StreetCotton pyjamasStreetNil before showerNil after showerStreetSwim suitStreetNilStreetNilStreet

Street

No. ofsamples

4242462 0461 01 0

28281616

54

72

No. ofindividuals

4242

1 01 01 0

1 01 0

2828999

72

Ratiomale/female

41 \1 4 /3-312-0 y

4-71ro/13I5 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. Itcan be calculated that, on the basis of differences in squame size, males ought to disperse about 1-25times as many squames as do females. The skin areas of the people studied by Noble & Davies wereavailable and, since the males were on average larger, a further factor of i-i6 might be added. Malesought then to disperse 1-45 times as many scales as do females; the sex ratio for dispersal of scales foundby Noble & Davies was 1-34. There is, however, a further factor to be taken into account when wediscuss 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, althoughmales dispersed about 3-5 times as many bacteria as do females, the sex difference disappeared ifallowance 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. Itseemed possible that this was under hormonal influence but examination of 100 post-menopausalwomen 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 malessignificantly outrank females. This male predominance does not extend to patients, however; studieson airborne staphylococci have failed to reveal differences between males and females in the degreeof dissemination in hospital wards (Lidwell & Brock, 1973). Some studies help to throw light on thisphenomenon. The classic work of Solberg (1965) showed that the degree of dispersal of Staph. aureuswas 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 exercisedin a cubicle, dispersal was mainly from below the waist. Recent studies in the Netherlands (Nobleet 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 wasmost significant for the abdomen and thighs in males and for the shin in the females (perhaps due tothe 'cheese-grater' effect of tights and stockings described by Mitchell & Gamble, 1974). If thisdifference is found to be true for studies of exercising rather than imdressing, the predominance ofmales in dispersing Staph. aureus might be ascribed simply to greater contamination of the thighs thanthe shins with perineal organisms.

There is still much that remains to be discovered in relation to dispersal. Why are males moreheavily colonized with skin bacteria than are females ? Why do some individuals without skin diseasecarry Staph. aureus on the skin for shortor longperiods ? Can differences in clothing accoimt fordifferences in dispersal pattern, and finally can dispersal of potential pathogens be prevented withoutrecourse to hot, perhaps uncomfortable, operating theatre clothing and without the application ofapparently harmful skin degerming compounds ?

Department of Bacteriology, W.C.NOBLESt John's Hospital for Diseasesof the Skin,Homerton Grove,London E9 6BX

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