Transference Hand Lip

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Journal of Applied Microbiology 2002, 93, 585–592

Comparative surface-to- hand and fingertip-to-mouth

transfer efficiency of gram-positive bacteria, gram-negative

bacteria, and phage

P. Rusin1*, S. Maxwel l

1and C. Gerb a

1

1University of Arizona, Department of Soil and Water Science, Building 38, Tucson, Arizona 85721 USA

2002 ⁄ 93 : received 4 March 2002, revised 17 May 2002 and accepted 27 July 2002

P . R U S I N , S . M A X W E L L A N D C . G E R B A . 2002.

Aims: To determine the transfer efficiencyof micro-organismsfrom fomites to hands and the

subsequent transfer from the fingertip to the lip.

Methods and Results: Volunteers hands were sampled after the normal usage of fomites

seeded with a pooled culture of a Gram-positive bacterium (M icrococ cusluteus), a Gram-

negative bacterium (Serratia rubidea)and phage PRD-1 (Period A). Activities includedwringing out a dishcloth ⁄ sponge, turning on ⁄ off a kitchen faucet, cutting up a carrot,

making hamburger patties, holding a phone receiver, and removing laundry from the washing

machine. Transfer efficiencieswere 38 Æ47% to 65 Æ80% and 27 Æ59% to 40 Æ03% for the phone

receiver and faucet, respectively.Transfer efficienciesfrom porous fomites were <0 Æ01%. In

most cases, M. luteuswas transferred most efficiently,followed by phage PRD-1 and S.

rubidea.When the volunteers’ fingertips were inoculated with the pooled organisms and held

to the lip area (Period B), transfer rates of 40 Æ99%, 33 Æ97%, and 33 Æ90% occurred with M.

luteus, S. rubidea,and PRD-1, respectively.

Conclusions: The highest bacteral transfer rates from fomites to the hands were seen with

the hard, non-porous surfaces. Even with low transfer rates, the numbers of bacteria

transferred to the hands were still high (up to 106 cells). Transfer of bacteria from thefingertip to the lip is similar to that observed from hard surfaces to hands.

Significance and Impact of the Study: Infectious doses of pathogens may be transferred to

the mouth after handling an everyday contaminated household object.

INTRODUCTION

The role of fomites in the transmission of disease remains

a controversial subject. Some epidemiological studies

have suggested that contaminated surfaces may play a role

in the spread of respiratory viruses (Hendley et al. 1973;Reed

1975;Hall et al. 1980)and laboratory studies have supported

this hypothesis. Other studies have implicated environmen-

tal surfaces in the transmission of bacteria (Manning et al.

2001; Ekanem et al. 1983; Bures et al. 2000; Manning et

al.

2001) However, the role of environmental surfaces in the

transmission of disease remains an issue of scientific debate

and fundamental information concerning the microbial

*Correspondence to: Patricia Rusin,Departmentof Soil, Water and Environmental,

Building38, University of Arizona, Tucson,Arizona, USA

(e-mail:

[email protected] i zona.edu).

ª 2002 The Society for Applied

Microbiology

mailto:[email protected]





transfer rates from environmental surfaces to the hands

and from the hands to the mouth remains scarce.

Separate studies have shown that microorganisms are

more efficiently transferred from nonporous than from

porous surfaces. Transfer of Escherichia coli from a laminate

surface to fingers was 40% up to two hours after the

contamination event (Scott and Bloomfield 1990a) while the

transfer efficiency of E. colifrom a damp cloth to the human

hand was only 0 Æ47% (Mackintosh and Hoffman 1984).

Bean et al. (1982) showed that viral transfer from poroussurfaces was poorer than from stainless steel although

percent transmission was not described. The efficacy of

transfer of rhinovirus from a donor’s fingertips to a

recipient’s hands via door knobs was as high as 22%

(Pancic et al. 1980). Studies do not provide direct

comparisons of the transmission rates from surfaces to

hands of bacteria and



586 P. RUSIN ET AL.

viruses. This information may be important to determine

which types of pathogens will be most affected by environ-

mental sanitation practices.

More quantitative information regarding the transmission

of viruses and bacteria from the fingertip to the lip is also

needed. This information is vital to understand the possiblerole of environmental surfaces and cross-contamination in

the transmission of disease. It is also important to establish

a basis for a risk assessment approach in the domestic

environment. Many infections are thought to arise within

the home. Although many of these infections are not life-

threatening, they do result in significant health care costs

(Bloomfield 2001). This study is the first to directly

compare Gram-positive bacteria, Gram-negative bacteria,

and viral transfer efficiency from porous and nonporous

fomites to the human hand and from the fingerpad to the

lip.

MAT E RIA L S A NDMETHOD S

The study consisted of two evaluation periods: A and B. In

Evaluation Period A, subjects’ hands were sampled follow-

ing contact with one of eight common surfaces that were

inoculated with a pool of three microorganisms comprising

Serratia rubideaAmerican Type Culture Collection (ATCC,

Rockville, MD) 11634, Micrococcus luteus ATCC 533, and

PDR-1 phage (J. Ito, University of Arizona). In Evaluation

Period B, subjects’ lower lips were sampled after they had

been touched with a fingertip that had been inoculated with

a pool of the same three microorganisms.

Subj ects

Subjects were healthy adults, aged 18–65 years. All

subjects signed informed consents as approved by the

University of Arizona Human Subjects Committee.

Con trol wash and disinfe ction proce dures

Prior to all study activities of Evaluation Periods A and B,

the following control wash was performed. Hands were

squirted with 70% ethanol for 10 s, subjects rubbed thealcohol thoroughly over their hands and wrists for 15 s, and

then hands were washed with 2 ml of liquid Ivory (Procter

and Gamble, Cincinnati, OH) for 30 s, rinsed for 15 s, and

dried on paper towels. Prior to sampling the lower lip, the

area was wiped for approximately 10 s with an alcohol

swab ⁄ wipe.

After all study sampling involving the prepared inoculum

of bacteria and phage, the following disinfection procedure

was performed. Subjects’ hands were squirted with 70%

alcohol for 10 s, the alcohol was rubbed over hand and wrist

surfaces for 15 s, and then hands were rinsed under running

tap water for 15 s and dried with paper towels. Subjects

then

conducted an Ivory soap-and-water wash for at least 30 s,

followed by a 30-s wash with Hibiclens

(4%

chlorhexidine gluconate; AstraZeneca, Wilmington, DE).

Subjects’ lower lips (Evaluation Period B) were disinfected

by twice wiping the area with an alcohol wipe (10 s

each) followed by swabbing with Hibistat (0 Æ5%

chlor hexidine gluconate; AstraZeneca, Wilmington, DE)

solution.

Preparati on of inocu lum

In each case, the inoculum was a pooled culture of S.

rubidea ATCC 11634, M. luteus ATCC 533, and PDR-1

phage. These organisms were chosen because they were

low risk to the subjects and the environment. The bacteria

were pigmented so they could be differentiated from the

normal flora. The pooled inoculum used on ⁄ in the fomites

consisted of approximately 108

CFU or PFU ml-1

of both types of bacteria and the phage. The pooled

inoculum used on the fingertip consisted of

approximately 106

CFU and PFU ml-1

. The bacteria

and phage in the pooled inoculum were enumerated daily

before use, using the spread-plate method for bacteria and

the agar-overlay method for phage as described in the

Enumeration and Incubation section below. The volumes

of inoculum used in ⁄ on the various fomites and on the

fingertips are described in the Microbial Transfer and

Sampling Procedures section.

The inoculum was prepared as follows. A frozen aliquot

of S. rubidea was transferred to Tryptic Soy broth (TSB,

Difco, Detroit, MI) incubated for 18 ± 2 h at 35 ± 2 C,

and streaked for isolation onto Tryptic Soy Agar (TSA,

Difco). An isolated colony was selected, transferred to a

tube of TSB, and incubated for 18 ± 2 h at 35 ± 2 C for

use in the study. The same procedure was used in the

preparation of the M. luteus culture. The PDR-1 phage

stock was prepared by adding the Salmonella typhimurium

LT2 (host bacterium) to TSB and incubating for 12–18 h

at 35 ± 2 C to bring the culture to a stationary phase. The

culture was brought to log phase by inoculating 1 ml of the

stationary phase culture into 100 ml TSB and incubating

for 2–3 h at 37 C on a rotating shaker table (150–

180 rev min-1

). Phage suspension (0 Æ1 ml) followed by log phase host culture (1 ml) was then added to top agar tubes

melted and maintained at 48 C. The inoculated top agar

tube was mixed and poured over a TSA plate, the

solidified agar overlay was inverted, and overlay plates

were incubated at 37 C for 24 h. After plaques were

confluent, TSB (5 ml) was added to each plate and

maintained at room temperature for 2 h to allow the

phage to diffuse through the solution. The TSB was

aspirated and centri- fuged lightly, after which the

solution was filtered using

0 Æ45 lm GN-6 filters (Gelman Sciences Inc., Ann Arbor,

MI), and the phage stock culture was stored at 4 C. Stock phage cultures were titrated 24 h before use. At each study



ª 2002 The Society for Applied Microbiology, Journal of Applied Microbiology, 93, 585–592



TRANSFER OF BACTERIA A ND PHAGE 587

start, the three cultures were pooled in TSB to achieve the

concentrations described above.

Microbial trans fer and sampli ng procedures

Evaluation period A. Transfer of microorganisms tohands from inoculated porous surfaces. Sampling was

performed after contact with six fomites ⁄ surfaces, which

had been inoculated with a pool of Serratia rubidea,

Micrococcusluteus, and PRD-1 coliphage. (approximately

108

CFU or PFU ml-1

of each organism). The fomites

were a sponge, a dishcloth, laundry, a carrot, and raw

ground beef. Prepar- ation and inoculation of the fomites

⁄ surfaces and subject contact procedures were as follows:

(1) Prior to inoculation, sponges (Scotch Brite, 3M, Mt.

Paul, MN) were boiled in Letheen broth (Difco, Detroit,

MI) for at least 1 h on three consecutive days. Each sponge

was saturated with 100 ml of pooled inoculum. Subjects

were asked to wring out the sponge for 10 s after which

the hands were allowed to dry for

1 m before sampling; (2) cotton dishcloths (30 · 30 cm,

Dayton Hudson, Minneapolis, MN) were rinsed in distilled

water and autoclaved. Each dishcloth was inoculated with

50 ml of pooled organisms. Subjects were asked to wring

out the dishcloth for 10 s after which subjects’ hands

were allowed to air dry for 1 min before sampling; (3) Each

load of laundry consisted of 10 swatches (100 cm2, either

100% cotton or 50 : 50 cotton ⁄ polyester blend, Hancock

Fabrics, Tucson, AZ). Swatches were weighed dry,

saturated with a known quantity of inoculum (100 ml for

the cotton blend and200 ml for the 100% cotton swatches), placed in the final

spin cycle of the washer, removed, reweighed, and the

remaining inoculum counts determined. Each subject trans-

ferred a load of laundry to the dryer. Subjects’ hands were

allowed to air dry for one min before sampling; (4) Carrots

were purchased at a grocery store (Kroger, Cincinnati,

OH), cut into four segments and gamma-irradiated at 25

kGy ⁄ min for 12 h, and kept frozen until the day of use to

maintain sterility. On the day of the test, carrots were

thawed and then dipped into the pooled inoculum. Subjects

were asked to cut the carrot into pieces, after which the

hand used to hold the carrot in place was allowed to air dry for 1 min before sampling. Seeded carrots were

assayed for density of microorganisms by immersing the

carrot into 40 ml of sterile physiological saline, vortexing

at high speed for 60 s, and enumerating the indicator

organisms as described in the Enumeration and

Incubation section; (5) Ground beef was purchased at a

grocery store (Kroger, Cincinnati, OH), gamma-

irradiated at 25 kGy ⁄ min for 12 h, and kept frozen until

the day of use to maintain sterility. The beef was

divided into 450-gram parcels and placed into a freezer

bag. A 23-ml aliquot of the pooled organisms in TSB was

added to each parcel. The parcel of ground beef was

kneaded for 10 min Subjects were asked to prepare four hamburger



patties from one pound (450 g) of inoculated ground beef

after which subjects’ hands were allowed to air dry for 1

min. The ground beef was assayed for the inoculum level

at the start and end of the study.

Transfer of microo rganisms to hands from inoculated

nonpor ous surfac es. A hard nonporous surface will not

absorb a known amount of inoculum such a porous surface

will. It was particularly difficult to apply a known volume

of pooled microorganisms to the round stainless steelfaucet handle due to runoff of the inoculum. Therefore, the

har d surfaces tested were inoculated by dipping the fomite

into a pool of the test organisms and allowing the inoculum

to air dry before handling. Sampling was performed after

contact with two surfaces that had been inoculated with a

pool of S. rubidea, M. luteus, and PRD-1 coliphage: a phone

receiver and a single-lever kitchen faucet handle. (1) The

area of the phone receiver to be handled by the subject

was marked. The phone receiver was disinfected with 70%

ethanol and allowed to dry, then dipped into the pooled

inoculum and allowed to air dry. Subjects were asked to

hold the receiver for 30 s as if answering the phone. The

hand was allowed to dry for 1 min and then sampled. Thearea of the receiver handled by the participant was also

sampled using a Dacron swab (Becton Dickinson, Sparks,

MD) and the density of indicator organisms determined;

(2) A single-lever faucet handle was disinfected with 70%

ethanol before and between each study use. The faucet

handle was dipped into a solution of pooled test organisms

in TSB and allowed to air dry. Each subject turned the

handle on and off twice. The hand used on the faucet

was allowed to air dry for

1 min and then sampled using a Dacron swab (Becton

Dickinson, Sparks, MD). The residual seeded microorgan-

isms on the faucet handle were also enumerated using a

Dacron swab. The density of each test organism in the

inoculum was determined in each case.

Evaluation period B. Transfer of microorganisms from

fingertip to lip. Sampling of each subject’s lower lip was

performed after 10-s contact with a fingertip that had been

inoculated with the pooled three-organism inoculum (ap-

proximately 106

CFU or PFU ml-1

) described above. A totalof 5 ll of inoculum was applied to the assigned finger and

allowed to air dry for 30 s. The subject then placed the

fingertip to the middle of the lower lip for 10 s. The

fingertip and area of contact on the lip were sampled using

Dacron swabs.

Bact erial sampling proc edureOne or both hands (per description) were sampled

following contact with the fomites, and the fingertip and

lip area were sampled in the hand-to-lip transfer.

Each sampling




588 P. RUSIN ET AL.

procedure was done with a Dacron swab moistened in 3 ml

of Letheen broth with the excess pressed out. Following

sampling, the swab(s) were returned to a tube of Letheen

broth and placed on ice for microbial enumerations. For

hand sampling, the swab was rubbed over the entire

ventral surface of the hand (including ventral surfaces of the thumb and fingers) twice, using opposite directions of

movement. When two hands were sampled, the two hands

were sampled separately and the swabs from both hands

were placed into a single tube of Letheen broth. The

fingertip was sampled by rubbing the swab over the

inoculated area of the fingertip, and the lip was sampled by

rubbing the swab over the area of the lip contacted by the

fingertip.

Enu meration and incubation

For enumeration of S. rubidea and M. luteus, samples

were plated and counted using the spread plate technique.

Samples were serially diluted to countable numbers and

plated onto duplicate plates of TSA. For phage analysis, the

overlay technique was used. Dilutions of phage suspension

(0 Æ1 ml) followed by log phase host culture (1 ml) was

added to melted top agar tubes, the inoculated top agar

tubes were mixed and poured over a TSA plate, the

solidified agar overlay was inverted, and overlay plates

were incubated at

37 C for 24 h. Plated samples were incubated aerobically

for

18–24 h at 35 ± 2 C, after which colonies typical of

M. luteus (lemon yellow) and S. rubidea (red) wereenumerated as were numbers of plaques of PRD-1. Num-

bers reported are the average of the counts from the plates

in the range of ‡25 to £ 250 CFU ⁄ PFU.

Numerical analys es

All microbial numerical results were converted to base 10

logarithms. The mean counts recovered from the hands ⁄

lip areas and fomites ⁄ fingertips were determined and

these mean counts were then used to evaluate transfer

efficiency using SAS version 6 Æ12.

RESULT S

Fomi te-to-ha nd tran sfer (Evalua tion Period A)

Table 1 summarizes the fomite-to-hand transfer results.

The Gram-positive bacterium, M. luteus, was transferred

more efficiently than the virus or phage, PRD-1, and the

Gram-negative bacterium, S. rubidea, from all but two

cases. The phage was the most efficiently transferred

organism from the carrot and the phone receiver. The

lowest transfer rates were consistently observed for S.

rubidea.

All three organisms were most efficiently transferred tothe hands from the phone receiver, the faucet handle and

the



carrot, in descending order. Transfer rates were always

higher from the dishcloth than from the sponge. Lower

transfer rates were consistently observed from the 50 : 50

cotton ⁄ polyester laundry swatches than from the 100%

cotton swatches. Although percent transfer was higher

from porous surfaces than from nonporous surfaces, the

levels of contamination of the hands were often very high

after handling porous fomites such as the dishcloth or the

sponge.

Fing ertip-t o-lip trans fer (Evalua tion Period B)

The fingertip-to-lip transfer results are summarized in

Table 2. As observed for surface-to-hand transfer, M. luteus

had the highest percent transfer from the fingertip to the

lower lip (40 Æ99%). However, the transfer efficiency of

S. rubidea was slightly higher than that observed for phage

PRD-1.

DISCUSSIO N

The possible role of fomites in the transmission of disease

requires further evaluation. In many nosocomialinfections, the route of transmission is not documented and

environmental surfaces are often not tested (Spender et

al. 1986; Cone et al. 1988). The role of fomites in the

domestic setting is even more difficult to assess. The

number of homes that would be required to statistically

evaluate the role of cross- contamination and cross-

infection would be prohibitive (Bloomfield 2001).

However, a first step that can be taken to assess the risk of

transmission from contaminated surfaces is to evaluate the

transfer efficiency rates of different types of bacteria and

viruses from surface-to-surface. This is the first study to

describe the transfer of two types of bacteria and a virus

from a variety of common household fomites to the hands.

The present study suggests that Gram-positive bacteriaare transmitted most readily from environmental surfaces

followed by viruses and Gram-negative bacteria. In a study

by Scott and Bloomfield (1990a), Staphylococcus aureusand

Escherichia coli were transferred from a laminate surface to

the fingertip at similar rates. Therefore, more research is

needed to determine whether Gram-positive bacteria are,

indeed, transferred more readily than Gram-negative bac-

teria or whether transmission rates from fomites are

organism specific.

Different survival rates may have influenced some of

these results. Survival rates of bacteria have been shown to

differ considerably (Perez et al. 1990; Snelling et al. 1991;

Falsey and Walsh 1993) and are even strain specific(Noskin et al.

1995; Neely and Maley 2000). Viral survival is also highly

variable (Hall et al. 1980; Mbithi et al. 1992; Adler 1996).

Although inocula were not allowed to dry for prolonged

periods, differential survival abilities may have influenced




Dishcloth

Sponge

9 Æ85

10 Æ44

5 Æ95

6 Æ46

0 Æ03

0 Æ02

FaucetCarrot

5 Æ837 Æ97

4 Æ705 Æ43

33 Æ470 Æ35

Hamburger

Phone receiver

Laundry – 100% cotton

8 Æ77

4 Æ92

8 Æ73

3 Æ93

4 Æ68

3 Æ63

0 Æ01

65 Æ80

<0 Æ01

Laundry – 50 : 50 cotton ⁄ polyester 8 Æ34 2 Æ71 <0 Æ01

Faucet

Carrot

6 Æ08

8 Æ97

5 Æ22

5 Æ85

27 Æ59

0 Æ12

Hamburger

Phone receiver

9 Æ91

6 Æ31

5 Æ12

5 Æ75

<0 Æ01 (0 Æ002)

38 Æ47

Laundry – 100% cotton

Laundry – 50 : 50 cotton ⁄ polyester

9 Æ79

9 Æ01

4 Æ40

3 Æ64

<0 Æ01 (0 Æ003)

<0 Æ01 (0 Æ0009)


Table 1 Results from fomite-to-hand transfer (Evaluation Period A)*

Mean log10 CFU or PFU

Organism ⁄ Type of fomite Level in ⁄ on fomite

Level recovered from

ventral surface of hands Transfer efficiency (%)

Micrococcusluteus

Dishcloth 10 Æ44 6 Æ90 0 Æ04

Sponge 9 Æ58 5 Æ98 0 Æ03

Faucet 6 Æ13 5 Æ59 40 Æ03

Carrot 9 Æ05 6 Æ31 0 Æ21

Hamburger 9 Æ79 5 Æ70 0 Æ06

Phone receiver 6 Æ60 6 Æ19 41 Æ81

Laundry – 100% cotton 9 Æ73 6 Æ17 0 Æ13

Laundry – 50 : 50 cotton ⁄ polyester 9 Æ39 5 Æ99 0 Æ06

PRD-1

Serratia rubidea

(0 Æ005)

(0 Æ0005)

Dishcloth 10 Æ34 5 Æ42 <0 Æ01 (0 Æ0045)

Sponge 11 Æ06 6 Æ50 <0 Æ01 (0 Æ0037)

* Number of subjects participating as follows: sponge, 100% cotton laundry, 50 : 50 cotton ⁄ polyester laundry – 10

each;

dishcloth – 11; hamburger, carrot, phone receiver, faucet handle )20each.

The CFU count for the fomite was calculated from the CFU per ml of the inoculum times the volume used to contaminate the fomite. For the

phone and faucet, CFU count for the fomite was the sum of the CFU count on the subject’s hand plus the CFU count recovered from the area of

the fomite handled by the subject.

Transfer efficiency ¼ (CFU count in ⁄ on hand ⁄ CFU count in ⁄ fomite) ·

100.

Table 2 Transfer efficiencyof bacteria and phage from hand to mouth* (Evaluation Period B)

Mean log10 CFU or PFU

Inoculum Placed Bacteria or phage Bacteria or phage recoveredOrganism on Fingertip recovered from lip from fingertip after transfer Transfer Efficiency (%)

Micrococcusluteus

PRD-1

Serratia rubidea

6 Æ63

5 Æ78

6 Æ66

5 Æ77

4 Æ69

5 Æ20

5 Æ97

5 Æ01

5 Æ54

40 Æ99

33 Æ90

33 Æ97

* 20 subjects participated in Period C.

Transfer efficiency ¼ [CFU count on lip ⁄ (CFU count on lip + CFU count recovered from transfer finger)] · 100.






590 P. RUSIN ET AL.

some of the results here although that is unlikely. Bacteria

have been shown to survive and even grow in damp

objects such as contaminated cloths and ground beef (Scott

and Bloomfield 1990b; Dickson and Olson 2001). In

addition, the seeded fomites in this study were handled by

volunteers within minutes of inoculation. Thereforedifferential survival or growth rates probably do not

account for the different transfer rates observed between

Gram-positive and Gram- negative bacteria from the

objects described here.

In this study, transfer efficiency from nonporous surfaces

was calculated differently than from porous surfaces. This

was a consequence of the nature of the two types of

surfaces. Porous surfaces can be inoculated with, and hold,

a known volume of pooled bacteria and phage. Most of a

measured volume of inoculum will run off of hard, smooth,

curved, nonporous surfaces. Hence transfer efficiency rates

must be calculated in a different manner for these two

types of surfaces. Transfer rates from hard, nonporous

surfaces were more efficient than from porous surfaces. A

porous surface, such as a sponge, offers many deep

recesses in which bacteria and viruses reside becoming

less accessible to the human hand. A hard smooth

surface does not offer crevices or passages in which

microorganisms may hide, hence higher transmission.

However, high levels of hand contamination occurred in

spite of poor transfer rates from some of the porous

fomites. After squeezing out a sponge or a dishcloth, the

subjects’ hands were highly contaminated.

These results suggest that commonly handled objects that

are microbially contaminated can serve as reservoirs of bacteria and viruses that can easily transfer to the hands

through direct contact, which in turn can be easily

transferred to the lip. Because of the seeding of these

fomites, concentrations of organisms are possibly higher

than what one would find in the household. However,

previous studies by the authors show that concentrations of

coliforms (which include opportunistic pathogens) are

sometimes quite high in the common household (Rusin

et al. 1998). These authors found that the water recovered

from the common kitchen sponge contained 6 Æ51 (log10)

coliforms per ml, reflecting very high numbers (approxi-

mately 3 Æ2

·

10

8

cells) in the sponge itself. In addition,early work (Davis et al. 1968) reported counts of E.

coli in domestic dishcloths of 107. Based on a 0 Æ0037%

transfer efficiency, 11 840 coliforms would be

transferred to the hand. Assuming 3 Æ2% (379) of these

bacteria are distributed on the fingertip, then 34% or 129

cells would be transferred into the mouth. This means

that if some members of Enterobacteriaceae, such as

Shigella or E. coli O157:H7, were in the dishcloth or

sponge in high numbers, infectious doses could easily be

transferred to the lip or mouth as low numbers of these

pathogens may cause disease (Dupont et al. 1989; Boyce

et al. 1995). It should also be remembered

that the risk of infection via a contaminated dishcloth is

heightened by multiple uses of the cloth during the day.

The high transfer rates seen in this study suggest that a

telephone receiver could also easily serve to transmit

disease. Large numbers of Salmonella may be excreted in

the stool of an infected person (up to 1010 Salm onella per gram of faeces (Feachem et al. 1983). Hence, if only

0 Æ001 g of residual stool were transferred from an infected

person’s contaminated hand to a telephone receiver, the

next user would have

107 104 Salm onella cells on the fingertip. If this were

placed in the mouth, the person would receive a dose of 36

383 cells that could easily result in disease (Blaser and

Newman

1982). The transmission of pathogenic bacteria via a

telephone receiver may be enhanced by multiple uses of

the telephone and by the fact that bacteria may survive for

hours on hard surfaces, especially when dried in naturalexcretions (Scott and Bloomfield 1990a; Snelling et al.

1991).

In comparison to bacteria, very little information is

available in the literature regarding the concentrations of

pathogenic human viruses in the domestic environment.

However, we do know that viruses can survive (remain

infectious) for hours to days on a hard surface (Ansari et

al.

1988; Brady et al. 1990), that low numbers of infectious

units have been shown to cause disease (Douglas 1970;

Ward et al. 1986), and that large numbers are often

found in human excretions (Gwaltney 2000; Rusin et

al. 2000). Hence, if a virus such as the rotavirus or Norwalk agent were on the surface of a fomite such as a

telephone receiver, infectious doses could easily be

transferred to persons handling the fomite under

ordinary circumstances. As an example, if a telephone

receiver were contaminated with a low concentration of

rotavirus agent (e.g. 10 000 infectious particles), 6580 of

these would be transferred to the hand during normal use

of the telephone with 211 of them found on the fingertip.

Our results with phage PRD-1 show that 72 infectious

particles could be ingested by the host, which could result

in disease since the infectious dose has been shown to be

as low as 1 PFU (Ward et al. 1986).Likewise, the faucet could also transmit the rhinovirus

from person to person. Gwaltney et al. (1978) found that

hand-to-hand transmission of this virus was a more

efficacious route of infection than the aerosol route and

the virus was often detected on the hands of volunteers. The

50% infectious dose (ID50) for this virus is less than one

50% tissue culture infectious dose (TCID50) (Douglas

1970). The transmission of rhinovirus from contaminated

surfaces has resulted in disease, as has been shown by

Gwaltney and Hendley (1982). These authors showed that

50% of recipients developed rhinovirus infection after

exposure to virus-contaminated coffee cup handles and

56% of volunteers became infected after exposure tocontaminated plastic tiles.







Food products may also bring pathogens into the home.

Cross contamination of kitchen surfaces by contaminated

meat products has been demonstrated (Dewit et al. 1979;

Deboer and Hahne 1990). Indeed, a variety of raw meats,

including raw ground beef (Daise et al. 1986; Gill et al .

1996), have been shown to be colonized by high numbersof bacteria (Shaw et al. 1987; Gill and Jones 1996; Ramos

and Lyon 2000). Little information is available assessing

bacterial levels on raw vegetables entering the home.

It is difficult to assess the risk of laundry as a fomite.

Certainly, the percent of seeded organisms transferred to the

hand was very small. However, in a recent study (Larson

and Gomez-Durate 2000), the use of a commercial laun-

dromat and the practice of not using bleach in the laundry

were the only two factors that correlated strongly with

disease transmission within the households of inner city

populations.

More quantitative information needs to be gathered to

evaluate the role of contaminated inanimate surfaces in the

domestic setting for disease transmission. In order to

perform a risk assessment in the domestic environment for

bacterial and viral pathogens we need more information

regarding: (1) occurrence and levels of potential pathogens

in homes (2) transfer efficiencies of various

microorganisms from surfaces to hands (3) survival times

of pathogens in natural secretions found in foods and

in ⁄ on inanimate objects (4) levels of pathogens secreted

by humans, and (5) infectious doses to perform risk

assessments in the household.

ACKNOWLED G E MENTS

This work was supported by Procter and Gamble, Cincin-

nati, OH. The authors would like to thank K. Wiandt,

W. Billhimer, J. Philippo and B. Keswick for their

assistance in preparing this manuscript.

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