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Bacterial occurrence in kitchen hand towels

September 2014
Food Protection Trends 34(5):312-317

Authors:

Akrum H Tamimi

The University of Arizona

Laura Sifuentes

The University of Arizona

Show all 6 authorsHide

The common occurrence of enteric bacteria in kitchen sponges and dishcloths suggests that they can play a role in the cross-contamination of foods, fomites and hands by foodborne pathogens. This study investigated the occurrence of bacteria in kitchen towels often used to dry dishes, hands and other surfaces in the domestic kitchen. A total of 82 kitchen hand towels were collected from households in five major cities in the United States and Canada and the numbers of heterotrophic bacteria, coliform bacteria, and Escherichia coli in each towel were determined. In addition, identification of the enteric bacteria was performed on selected towels. Coliform bacteria were detected in 89.0% and E. coli in 25.6% of towels. The presence of E. coli was related to the frequency of washing.

. Average geometric means of bacteria found in kitchen towels (log 10 CFU or MPN/towel) collected from various cities

…

Average arithmetic mean of bacterial populations found on kitchen hand towels (CFU or MPN) collected from various cities

…

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Content uploaded by Akrum H Tamimi

Content may be subject to copyright.

Food Protection Trends September/October

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*Corresponding author: Phone: +1 520.621.6906; Fax: +1 520.621.6366; E-mail: gerba@ag.arizona.edu

ABSTRACT

The common occurrence of enteric bacteria in kitchen

sponges and dishcloths suggests that they can play a

role in the cross-contamination of foods, fomites and

hands by foodborne pathogens. This study investigated

the occurrence of bacteria in kitchen towels often used

to dry dishes, hands and other surfaces in the domestic

kitchen. A total of 82 kitchen hand towels were collected

from households in ﬁve major cities in the United States

and Canada and the numbers of heterotrophic bacteria,

coliform bacteria, and Escherichia coli in each towel

were determined. In addition, identiﬁcation of the enteric

bacteria was performed on selected towels. Coliform

bacteria were detected in 89.0% and E. coli in 25.6%

of towels. The presence of E. coli was related to the

frequency of washing.

INTRODUCTION

Several studies have documented the common occurrence

of large populations of heterotrophic and enteric bacteria in

kitchen sponges and dishcloths (1, 2, 5, 8), where the moist

environment and collected food residues create an ideal

environment for the growth of bacteria. Enriquez et al. (2)

found total and fecal coliform bacteria in large numbers in

cellulose sponges and dishcloths, sometimes reaching levels

greater than 106 colony-forming-units (CFU) per ml in uid

squeezed from these cleaning tools. Salmonella spp. was

isolated from almost 14% of the dishcloths. Sco et al. (8)

documented the occurrence of E. coli in kitchen towels, and

Maick et al. (4) reported isolation of Camplyobacter from

tea towels in the kitchen aer preparation of meals made

with poultry. Sco and Bloomeld (6) documented the

survival of Salmonella and E. coli in coon kitchen cloths and

suggested they may play a role in cross-contamination in the

home environment. e goal of this study was to assess the

occurrence of total and enteric bacteria in kitchen towels as it

relates to environmental and towel cleaning.

1Dept. of Soil, Water and Environmental Science,

University of Arizona, Tucson, AZ 85721, USA

2Kimberly-Clark Corporation, 2100 Winchester Road,

Neenah, WI 54956, USA

Charles P. Gerba,1* Akrum H.

Tamimi,1 Sherri Maxwell,1 Laura Y.

Sifuentes,1 Douglas R. Hoffman2

and David W. Koenig2

PEER-REVIEWED ARTICLE

Food Protection Trends, Vol 34, No. 5, p.312-317

6200 Aurora Ave., Suite 200W, Des Moines, IA 50322-2864

Bacterial

Occurrence in

Kitchen Hand

Towels

foodprotection.org Food Protection Trends 313

MATERIAL AND METHODS

e study was conducted in ve major cities in North

America: Chicago, IL; Tucson, AZ; New Orleans, LA;

Orlando, FL and Toronto, ON, Canada. e numbers of

towels collected from each city is presented in Table 1. ese

cities represent dierent weather conditions, varying from

cold to hot and from dry to humid.

Random households were selected in each city and towels

were collected by going door to door and requesting one

used towel from the kitchen. A survey of household towel

use and characteristics also was conducted for each house

selected. e information was obtained from the person in

the household who provided the towel. A total of 82 kitchen

towels were collected.

e questions in the survey were related to towel use and

frequency of cleaning. ese questions identied: age of

towel in months, frequency of washing of towel in days per

month, towel frequency of use, and the number of days since

the towel was last washed.

Each collected and used kitchen towel was submerged

in peptone broth (Difco, Sparks, MD) to extract bacteria

from the towel. Each towel was placed in a stomacher bag

with either 500 or 250 ml of peptone broth, based on towel

size and the material’s absorbance, to guarantee full soaking

of the towel. Each towel was then manually kneaded in the

peptone broth (Difco, Sparks, MD) for ve minutes until

the broth was completely absorbed by the towel. e broth

was extracted from the towel by wringing the liquid out by

pressing it against two stainless steel metal plates (AK Steel,

Cincinnati, OH). e extract or dilution (10-fold dilutions in

peptone broth) was plated on selective media for isolation of

the various bacterial populations.

Each towel was tested for total bacteria (heterotrophic

bacteria counts; HPC), coliform bacteria, and Escherichia

coli. HPC were assayed by spread plating on R2A media

(Difco, Sparks, MD) or aer dilution (in phosphate buered

saline). Aer incubation for 5 days at 25°C, viable colonies

were counted. Coliforms and E. coli were assayed by the most

probable number (MPN) method, using the Colilert Quanti-

tray method (IDEXX; Westbrook, ME), and enumerated

aer incubation at 35°C for 24 hours. A maximum of 100

ml of the towel extract could be assayed by this method.

Selected coliforms and presumptive E. coli isolates from

randomly selected towels were picked from petri plates and

identied by use of API bacterial identication test kits 20E

(bioMérieux, Marcy-l’Etoile, France).

e average area of the kitchen towels, for all cities, was

calculated to be about 1000 cm2, with a standard deviation of

150 cm2. erefore, it was decided to do all analyses on a per

towel basis.

A database was developed, and all collected data from the

survey and the laboratory analytical data were entered in the

database (see Tables 1 through 3). Data were manipulated in

various manners and multiple analyses of variance (ANOVA)

were conducted on the data to assess relationships between

demographics and characteristics of the towels and their use.

Microso Excel was used for the analysis (Microso Corp.,

Redmond, WA). A completely randomized design was used

to perform the ANOVA, with a rejection region of 5% using

the F distribution.

RESULTS

e results for overall occurrence of the studied bacteria

are presented as both arithmetic and geometric averages

TABLE 1. Average arithmetic mean of bacterial populations found on kitchen hand towels

(CFU or MPN) collected from various cities

City HPC* Coliforms E. coli

Mean St. Dev n Mean St. Dev n Mean St. Dev n

Chicago 2.98E + 08 6.12E + 08 19 4.76E + 03 1.10E + 04 20 6.00E + 00 1.92E + 01 20

Tucson 1.62E + 08 2.31E + 08 19 2.55E + 06 1.11E + 07 20 1.51E + 03 6.73E + 03 20

New Orleans 9.42E + 08 1.19E + 09 4 5.50E + 03 4.02E + 03 4 1.05E + 01 1.33E + 01 4

Orlando 8.30E + 07 1.38E + 08 18 3.97E + 05 8.64E + 05 19 7.24E + 03 1.68E + 04 19

Toronto 9.49E + 07 2.22E + 08 19 1.04E + 04 2.24E + 04 19 1.34E + 00 4.80E + 01 19

Average/Total 3.16E + 08  79 5.93E + 05  82 1.75E + 03  82

*HPC: Heterotrophic Plate Count

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314

(Tables 1 and 2). Figure 1 shows that all kitchen towels for

the 5 cities had at least 1 × 103 CFU/towel, and some had

HPC greater than 1 × 109 CFU/towel. e overall average

was 3.16 × 108 CFU/towel. At least one MPN of coliform

bacteria was found on towels collected from most cities, and

values higher than 1 × 106 MPN were observed in two cities

(Tucson and Orlando).

E. coli concentrations on kitchen towels were about one

MPN per towel, but values as high as 1 × 104 CFU/towel were

observed in some cities. Coliform bacteria were detected in

almost all of the towels (89.0%) and E. coli in 25.6%.

e highest numbers of bacteria per towel were found in

those collected from New Orleans and the lowest in towels

collected from Orlando (Table 1 and Fig. 1). Tucson had the

TABLE 2. Average geometric means of bacteria found in kitchen towels

(log10 CFU or MPN/towel) collected from various cities

City HPC* Coliforms E. coli

Geo. Mean St. Dev n Geo. Mean St. Dev n Geo. Mean St. Dev n

Chicago 6.8 1.9 20 2.0 1.4 20 0.3 0.4 20

Tucson 7.6 1.3 20 3.4 1.8 20 0.4 1.0 20

New Orleans 8.3 1.1 4 3.7 0.3 4 0.7 0.7 4

Orlando 7.3 1.4 19 3.9 2.1 19 1.6 1.7 19

Toronto 6.1 1.7 19 2.8 1.4 19 1.3 0.5 19

Average/Total 7.2  82 3.2  82 0.9  82

*HPC: Heterotrophic Plate Count

TABLE 3. Statistical differences between parameters studied for kitchen towels collected

in the study

Parameter HPC* Coliforms E. coli

Between cities <0.009 <0.006 <0.0003

Age of towel

(<12 or >12 months) 0.446 0.481 0.424

Frequency of washing

(<3 or >4 days) 0.675 0.351 0.014

Frequency of use

(<7 times a day or >8) 0.012 0.981 0.780

Last time washed

(1 day vs. >2) 0.066 0.321 0.172

*HPC: Heterotrophic Plate Count

Note: Bold and underlined values indicate signicant dierences (P < 0.05).

foodprotection.org Food Protection Trends 315

FIGURE 1. Distribution of heterotrophic plate counts (HPC) found in kitchen towels

collected om various cities; each value represents an individual towel.

Sample ID

HPC (MPN/Towel)

1.0E+10

1.0E+09

1.0E+08

1.0E+07

1.0E+06

1.0E+05

1.0E+04

1.0E+03

0 5 10 15 20

FIGURE 2. Distribution of coliform bacteria numbers found on kitchen towels collected om

various cities; each value represents an individual towel.

Sample ID

Coliforms (MPN/Towel)

1.0E+08

1.0E+07

1.0E+06

1.0E+05

1.0E+04

1.0E+03

1.0E+02

1.0E+01

1.0E+00

0 5 10 15 20

Food Protection Trends September/October

316

FIGURE 3. Distribution of E. coli found on kitchen towels collected om ve of the cities studied;

each value represents an individual towel.

Sample ID

E.coli (MPN/Towel)

1.0E+05

1.0E+04

1.0E+03

1.0E+02

1.0E+01

1.0E+00

1.0E-01

0 5 10 15 20

highest numbers of coliform bacteria in the towels, followed

by number of E. coli isolated from towels collected in Orlando

(Table 1 and Figures 2 and 3).

Because the distribution of the bacteria exhibited a log

normal distribution, it was log transformed for further

analysis (Table 2). ere was a statistically signicant

relationship between city of collection and all types of

bacteria isolated. Frequency of use was related to the

numbers of HPC, while the concentration of E. coli was

related to the frequency of washing. In addition to E. coli,

other bacteria identied in the towels included Enterobacter

cloacae, Klebsiella pneumonia and K. oxytoca.

DISCUSSION

is is the rst study to address the concentrations and

types of enteric bacteria in kitchen hand towels. Sco et al.

(8) studied the occurrence of bacteria in kitchen towels in

the United Kingdom but sampled the surfaces only by use of

Rodac plates. In that study, E. coli was detected in 1.9% and

coliforms in at least 4.1% of the kitchen towels. e genera

of bacteria detected in their study were similar to the ones

observed in the present study. We detected coliforms in

89.0% and E. coli in 25.6% of the towels. e greater numbers

we observed are most likely because we extracted the bacteria

from the towel using an eluent to obtain a total count of the

bacteria on and within the towel.

e relationship between the numbers of bacteria and

the dierent cities (excluding New Orleans, since it had so

few samples) was statistically signicant, which may reect

climate and dierent use paerns or types of food prepared.

Statistically signicant lower numbers of HPC occurred in

towels that were washed less (Table 3). E. coli numbers also

were related to the frequency of washing, with numbers on

towels being lower the more oen they were washed. Age of

the towel and days since last time washed did not inuence

the concentration of any of the bacteria in the towels. e

results suggest that E. coli is particularly easily removed

during washing or requires an unusually long time to colonize

and grow in the towels. Coliforms, E. coli and Salmonella can

survive the drying of kitchen cleaning cloths and regrow if

the cloth becomes soiled again (3).

Maick et al. (4) also reported the isolation of Camplyo-

bacter from a kitchen towel of a domestic kitchen aer prepa-

ration of chicken naturally contaminated with the organism.

e researchers aributed the isolation of this pathogen

to poor hand washing, followed by wiping of the dirty

hands aer handling the chicken. e same group reported

cross contamination of dishes when wiped dry with towels

contaminated with E. coli O157:H7, Salmonella or Campy-

lobacter jejuni (4). e researchers recommended frequent

replacement or decontamination of kitchen towels. Sco and

Bloomeld (7) reported that detergent washing and drying of

kitchen cloths in the kitchen only slightly reduced microbial

foodprotection.org Food Protection Trends 317

contamination, and regrowth occurred within 24 hours, since

the towels remained damp. e researchers demonstrated

that soaking the cloths in 4,000 mg/L of bleach for two

minutes was more eective in reducing bacterial numbers;

however, not all the cloths could be decontaminated,

probably because of dierences in organic load.

is current study demonstrated that signicant numbers

of coliform and E. coli commonly occur in kitchen towels.

ese results also demonstrate the potential for cross-

contamination of foodborne enteric bacterial pathogens

and their growth in kitchen towels.

1. Chaidez, C., and C. P. Gerba. 2000.

Bacteriological analysis of cellulose sponges

and loofahs in domestic kitchens from a

developing country. Dairy, Food Environ.

Sanit. 20:834–837.

2. Enriquez, C. E., R. Enriquez-Gordillo,

D. I. Kennedy, and C.P. Gerba. 1996.

Bacteriological survey of used cellulose

sponges and dishcloths from domestic

kitchens. Dairy, Food Environ. Sanit. 17:20–24.

3. Maick, K., K. Durham, G. Domingue,

F. Jorgensen, M. Sen, D. W. Schaner, and

T. Humphrey. 2003a. e survival of

foodborne pathogens during domestic

washing-up and subsequent transfer onto

washing-up sponges, kitchen surfaces and

food. Intl. J. Food Microbiol. 85:213–226.

4. Maick, K., K. Durham, M. Hendriz, J. Slader,

C. Grin, M. Sen, and T. Humphrey. 2003b.

e microbiological quality of washing-up

water and the environment in domestic

and commercial kitchens. J. Appl. Microbiol.

94:842–848.

5. Rusin, P., P. Orosz-Coughlin, and C. P. Gerba.

1998. Reduction of faecal coliform, coliform

and heterotrophic plate-count bacteria in

the household kitchen and bathroom by

disinfection with hypochlorite cleaners.

J. Appl. Microbiol. 85:819–828.

6. Sco, E., and S. F. Bloomeld. 1990a.

e survival and transfer of microbial

contamination via cloths, hand and utensils.

J. Appl. Bacteriol. 68:271–278.

7. Sco, E., and S. F. Bloomeld. 1990b. Invest-

igations of the eectiveness of detergent

washing, drying and chemical disinfection

on contaminated of cleaning cloths. J. Appl.

Bacteriol. 68:279–283.

8. Sco, E., S. F. Bloomeld, and C. G.

Barlow. 1982. An investigation of microbial

contamination in the home. J. Hyg. Camb.

89:279–293.

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Poor hand hygiene contributes to diarrhea in developing countries. Handwashing with soap reduces diarrhea risk, but drying hands on contaminated towels can compromise the benefits of handwashing. In response to the challenge of keeping hands clean, an antimicrobial hand towel was developed and shown to be promising in the laboratory, but has not been adequately tested in the field. We evaluated the effectiveness of an antimicrobial towel in two randomized, double-blinded crossover trials among mothers with children<5 years old in 125 households in western Kenya. In trial 1, we randomly assigned mothers to use either the treated towel or an identical untreated (placebo) towel and made surprise home visits at random times once a week for three weeks. At each visit, we tested hands for Escherichia coli using sterile hand rinses, then switched towel types in the two groups and repeated three weekly rounds of E. coli testing. In crossover trial 2, we compared E. coli contamination of maternal hands immediately following three different handwashing/drying procedures: soap and water þ treated towel, water only þ treated towel, and soap and water þ air dry. There was no statistically significant difference in the level of E. coli contamination on maternal hands by type of towel used during trial 1 (odds ratio for treated vs untreated towel: 1.14, 95% confidence interval 0.83e1.56). In trial 2, there were no significant differences in E. coli contamination of maternal hands by handwashing/drying procedure. In these trials, use of antimicrobial hand towels did not prevent E. coli contamination of mothers’ hands in Kenyan households during random testing and offered no advantages over standard handwashing and drying practices. Handwashing with soap and clean water and drying with clean towels are recommended.

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Handwashing with soap is an effective and economical means to reduce the likelihood of Escherichia coli infection from indirect contact with contaminated surfaces during food preparation. The purpose of this study was to conduct a quantitative microbial risk assessment (QMRA) to evaluate the risk of infection from indirect contact with fomites contaminated with E. coli after hand washing with antimicrobial hand soaps. A Monte Carlo simulation was done with a total of 10,000 simulations to compare the effectiveness of two antimicrobial and one control (non-antimicrobial) bar soaps in reducing the exposure and infection risk compared to no hand washing. The numbers of E. coli on several fomites commonly found in household kitchens, as well as the transfer rates between fomites and onto fingertips, were collected from the literature and experimental data. The sponsor company provided the E. coli survival on hands after washing with antimicrobial and control soaps. A number of scenarios were evaluated at two different exposure doses (high and low). Exposure scenarios included transfer of E. coli between meat-to-cutting board surface-to-hands, meat-to-knife surface-to-hands, and from a countertop surface-to-hands, kitchen sponge-to-hands, hand towel-to-hands, and dishcloth-to-hands. Results showed that the risks of illness after washing with the control soap was reduced approximately 5-fold compared to no handwashing. Washing with antimicrobial soap reduced the risk of E. coli infection by an average of about 40-fold compared with no handwashing. The antimicrobial soaps ranged from 3 to 32 times more effective than the non-antimicrobial soap, depending on the specific exposure scenario. Importance: The Centers for Disease Control and Prevention indicate the yearly incidence rate of Shiga Toxin producing E. coli infections is about 1.7/100,000, with about 10% of cases leading to life-threatening hemolytic uremic syndrome and 3-5% leading to death. Our findings confirm handwashing with soap reduces the risks associated with indirect transmission of E. coli infection from contact with fomites during food preparation. Further, in these exposure scenarios, antimicrobial soaps were more effective overall than the non-antimicrobial soap in reducing exposure to E. coli and risk of infection.

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An investigation of the bacterial flora in over 200 homes is reported. The occurrence of potential pathogens and the levels of contamination at individual sites, particularly in the kitchen, toilet and bathroom is described and the implications for hygiene practices in the home discussed.

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Jan 2000

Bacteriological survey of used cellulose sponges and cotton dishcloths from domestic kitchens

Article

Jan 1997

The Survival and transfer of microbial contamination via cloths, hands and utensils

Article

Apr 1990
J Appl Bacteriol

Survival and transfer of bacteria from laminated surfaces and cleaning cloths were investigated under laboratory conditions. Drying produced substantial reductions in numbers of recoverable organisms and achieved satisfactory decontamination of clean laminate surfaces. On soiled surfaces and on clean and soiled cloths, Gram-positive and some Gram-negative species survived for up to 4 h, and in some cases up to 24 h. Where contaminated surfaces or cloths came into contact with the fingers, a stainless steel bowl, or a clean laminate surface, organisms were transferred in sufficient numbers to represent a potential hazard if in contact with food.

Investigations of the effectiveness of detergent washing, drying and chemical disinfection on contamination of cleaning cloths

Article

Apr 1990
J Appl Bacteriol

Detergent washing, drying and chemical disinfection for decontamination of cleaning cloths was investigated with cloths contaminated by use in the domestic environment. Detergent washing produced only limited reductions in microbial contamination and cloths then stored at room temperature for 24 h showed increases in contamination due to multiplication of residual survivors. For effective and consistent decontamination of cloths, detergent washing followed by drying at 80 degrees C for 2 h was required. Hypochlorite and phenolic disinfectants produced significant reductions in contamination, but chemical disinfection may be unreliable where cloths are heavily contaminated.

Reduction of faecal coliform and hetertrophic plate count bacteria in the household kitchen and bathroom by disinfection with hypochlorite cleaners

Article

Dec 1998

Fourteen sites evenly divided between the household kitchen and bathroom were monitored on a weekly basis for numbers of faecal coliforms, total coliforms and heterotrophic plate count bacteria. The first 10 weeks comprised the control period, hypochlorite cleaning products were introduced into the household during the second 10 weeks, and a strict cleaning regimen using hypochlorite products was implemented during the last 10 weeks. The kitchen was more heavily contaminated than the bathroom, with the toilet seat being the least contaminated site. The highest concentrations of all three classes of bacteria were found on sites that were moist environments and/or were frequently touched; these included the sponge/dishcloth, the kitchen sink drain area, the bath sink drain area, and the kitchen faucet handle(s). The implementation of a cleaning regimen with common household hypochlorite products resulted in the significant reduction of all three classes of bacteria at these four sites and other household sites.

The microbiological quality of dishwater and the environment in domestic and commercial kitchens

Article

May 2003

To determine the microbiological quality of washing-up water and the environment in domestic and commercial kitchens. Chicken meals were prepared by people without food safety training in their own kitchen (n = 52) or by trained staff in a commercial kitchen (n = 10). Study participants then washed-up, cleaned the kitchen and completed a food hygiene questionnaire. The temperature and microbiological quality of the washing-up water, and the presence of pathogens in dishcloths, tea towels and other kitchen samples was determined. Of the raw chickens used in meal preparation, 96 and 13% were naturally contaminated with Campylobacter or Salmonella spp., respectively. In domestic kitchens, two of 45 sponges, dishcloths or scourers and one of 32 hand- or tea towels were contaminated with Campylobacter after washing-up and cleaning but none of the tap or sink swabs yielded pathogens. The mean washing-up water temperature in the domestic kitchens was 40.7 degrees C, whereas in the commercial kitchen it was 44.7 degrees C (P = 0.04). Study participants who used hotter water (>/=40 degrees C) had lower levels of bacteria in their washing-up water. The aerobic plate counts of the washing-up water samples in domestic homes were usually between 105 and 106 CFU ml-1 but those associated with the commercial kitchen were consistently lower (P = 0.01). Despite this, Campylobacter was detected in one of 10 washing-up water samples from the commercial kitchen but in none of the samples from domestic kitchens. Pathogenic microorganisms can be recovered relatively frequently from the kitchen environment. By identifying factors that affect the number of microorganisms in washing-up water and the kitchen environment, evidence-based recommendations on implementing domestic food hygiene can be made.

The survival of foodborne pathogens during domestic washing-up and subsequent transfer onto washing-up sponges, kitchen surfaces and food

Article

Sep 2003
INT J FOOD MICROBIOL

In this study, the survival of Salmonella, Campylobacter and Escherichia coli O157: H7, when exposed to a range of constant temperatures (47-60 degrees C), in hard or soft water, in the presence/absence of detergent (0-0.3%) and organic matter, and during drying, was investigated. Further experiments used a washing-up process simulation, where soiled dishes contaminated with bacteria were washed in a bowl of warm water containing detergent. In addition, this study considered the risk of bacterial transfer onto (1) sterile dishes and sponges via contaminated water, (2) kitchen surfaces wiped with a contaminated sponge, (3) items placed in direct contact with a contaminated kitchen surface, (4) food placed on a contaminated dish or (5) dishes from contaminated food. A proportion of dishes remained contaminated with all pathogen types after a typical washing-up. Water hardness did not appear to affect survival. E. coli, and to a lesser extent Salmonella, survived towel- or air-drying on dishes and after towel-drying the cloth became contaminated on every occasion, regardless of the test organism. A proportion of sterile dishes washed after contaminated dishes became contaminated with pathogens but transfer from dishes onto food was rare. Washing-up sponges frequently became contaminated with pathogens. The results of this study highlight the potential for survival and cross contamination of food borne pathogens in the kitchen environment.