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Journal of Food Engineering 80 (2007) 885–891

Efficiency of manual dishwashing conditions on bacterial survivalon eating utensils

Jaesung Lee a, Richard Cartwright b, Tom Grueser b, Melvin A. Pascall a,*

a Department of Food Science and Technology, Ohio State University, 2015 Fyffe Road, Columbus, OH 43210, USAb Hobart Corporation, 701 S. Ridge Avenue, Troy, OH 45374, USA

Received 11 April 2006; received in revised form 8 August 2006; accepted 9 August 2006Available online 6 October 2006

Abstract

This study evaluated the sanitization efficacies of manual three-compartment dishwashing processes as a function of washing temper-ature/time, contaminating organic matter, sanitizing condition, and bacterial type. Ceramic plates, drinking glasses, stainless-steel forks,spoons and knives and plastic serving trays were contaminated with egg, cheese, jelly, lipstick and milk. Each was inoculated with E. coli

and L. innocua. Greater than 5-log bacterial reductions were achieved for all samples after washing at the combination of low washingtemperature (24 �C) and minimal sanitizer concentration (150 ppm), except for bacteria on the milk-contaminated regular glasses. Theviability of the bacterial species was affected by both organic matter types and the washing water temperature. Although E. coli showedbetter survival when compared with L. innocua for jellied utensils, there was no significant difference in survival between them for allother washing conditions. The use of quaternary ammonium compounds had similar killing effect against both bacteria.� 2006 Elsevier Ltd. All rights reserved.

Keywords: E. coli; Listeria innocua; Manual dishwashing; Bacterial survival; Eating utensils

1. Introduction

Pathogens can be transferred to food from utensils thatare not properly cleaned and sanitized. Since some patho-genic microorganisms can survive outside the human bodyfor considerable periods of time, unsanitized utensils couldbe a direct or indirect source of food borne illnesses (FoodCode, 2001a). A 2003 US Food and Drug Administration(FDA) report on the occurrence of foodborne illness riskfactors in retail food establishments mentioned the needfor improvement in the sanitization process for food con-tact surfaces (FDA, 2004). This report documented theseobservations after data were collected from over 900 foodestablishments. The data showed that out of compliancepercentages remained high for issues relating to: (1) impro-per food holding time and temperature; (2) poor employeepersonal hygiene; and (3) contaminated equipment. Of the

0260-8774/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.jfoodeng.2006.08.003

* Corresponding author. Tel.: +1 614 292 0287; fax: +1 614 292 0218.E-mail address: pascall.1@osu.edu (M.A. Pascall).

data collected, improper cleaning and sanitizing of foodcontact surfaces was the item most commonly observedto be out of compliance.

The washing protocols for automatic dishwashers usingonly hot water or a water–chemical combination arereported in documents prepared by the NSF International(ANSI/NSF, 2001). These standards also mandate theeffective heat load measurements for an efficient water san-itizing automatic dishwasher. This means that a hotenough temperature must be reached for a long enoughperiod of time to sanitize the utensils. Different time/tem-perature combinations are effective in killing germs. Thistime/temperature relationship is measured in Heat UnitEquivalents (HUEs). To fulfill this ANSI/NSF standard,Stahl Wernersson, Johansson, and Hakanson (2004b)reported that the removal of all visible soil and detergentfrom utensils, and >3600 HUEs must be achieved in wash-ing tests using Mycobacterium phlei in milk and in culturebroth. HUE testing is a method of ascertaining the effectof the cumulative killing factors applied to dish surfaces

886 J. Lee et al. / Journal of Food Engineering 80 (2007) 885–891

from time and temperature exposure in dishwashers.Chemical sanitizing equipment on the other hand, shouldproduce a 5-log reduction in bacterial species inoculatedonto eating utensils that are subjected to washing at mod-erately hot temperatures (>49 �C). Although the FDAFood Code (2001 b) specifies that the temperature of thewashing zone in manual washers should be P43 �C, thiscondition is sometimes not maintained because of itsuncomfortable nature and a reluctance by dishwashingemployees to wash utensils at these high temperatures(Pfund, 2004). Therefore, there is a need to establish utensilwashing protocols that can result in the 5-log reductionunder conditions that are more comfortable for theseemployees. As a result, this study begins a process of exam-ination of several manual dishwashing protocols and willattempt to discover the ones that would result in the 5-log reduction at temperatures lower than 43 �C.

Another reason for the establishment of these protocolsis the fact that NSF International does not have writtenperformance requirements for manual dishwashing whencompared to the detailed protocols that exist for automaticwashers. However, to perform at optimum efficiency, amanual dishwasher’s sanitizing protocol should employ acombination of proper washing conditions and the appro-priate concentration of an effective sanitizer in order toachieve the required 5-log bacterial reduction. To test theefficiency of the dishwashing protocol in our study, weselected ceramic plates, drinking glasses (regular and wineglasses), stainless-steel cutleries (knives, forks and spoons)and plastic serving trays to estimate the potential of a man-ual dishwashing process to remove organic contaminantsinoculated with Escherichia coli and Listeria innocua. Theseutensils were chosen because they are widely used bypatrons in restaurants.

Manual dishwashing is subject to fluctuations in its effi-ciency to remove microorganisms from eating utensils. Thisefficiency could be affected by the number and sizes of uten-sils, the time designated to clean them, the initial microbialload, quality of the detergent, the nature of the organicmatter on the utensils, washing temperature, the attitudeof the employee and the complexity of the utensils to becleaned (Mattick et al., 2003b; Montville, Chen, & Schaff-ner, 2002).

The objectives of this study were to evaluate the saniti-zation efficacies of three-compartment manual dishwashingprocesses on selected utensils as a function of washing tem-perature, contaminating organic matter, sanitizing concen-tration/time, and types of bacterial strains.

2. Methods and materials

2.1. Bacterial sample

Escherichia coli K12 (ATCC 29181) and L. innocua See-liger (ATCC 33090) were used during this study. The cul-tures were stored frozen (�80 �C) in 30% (v/v) sterileglycerol. When required for testing, a loopful of each

organism was revived in 10 ml Trypticase soy broth supple-mented with 0.3% (w/w) yeast extract (TSBYE) and incu-bated at 37 �C for 18 h. A loopful of broth from this wasinoculated on a Tryptic soy agar with a 0.3% (w/w) yeastextract (TSAYE) slant and incubated for 18 h at 37 �C.The cells grown on the slant were stored at 3 �C and usedas a stock culture. At each experiment, a loopful of thisstock culture was transferred to 70 ml TSBYE and incu-bated at 37 �C until the final concentration of cells in themedium reached about 9.0 · 108 cfu ml�1 for E. coli and1.3 · 109 cfu ml�1 for L. innocua. Cells in the broth wereharvested by centrifugation at 10,000g for 10 min at 4 �C.The supernatant was discarded and the pellets were resus-pended in 70 ml sterile deionized potassium phosphate buf-fer (pH 7.2). Each cell suspension was separately mixedwith each of the food samples to be tested in this study.

2.2. Preparation of the food samples

The contaminating organic matter (food items) used inthis study were semi-solid cream cheese (15% fat), wholeraw eggs, sugar-free orange flavored jelly, red colored lip-stick, and grade A pasteurized milk (8% fat). All food itemswere purchased from a local store the day before eachexperiment and kept at 4 ± 1 �C. The food items werenot sterilized. However, except for the milk, there was noevidence of microbial growth on the TSAYE plated 10�1

diluted (w/w) food items. No microbial growth in the milksample on MacConkey agar (Difco, Detroit, MI) for E. coli

and Modified Oxford agar (Difco, Detroit, MI) for L. inno-cua, indicated that colonies seen on TSA were not our tar-get bacteria. Furthermore, a comparison of the colonycounts from the TSAYE with that of the selective agarsafter washing ensured that those recovered were the sameones that were inoculated. Therefore, the bacterial recoverydata from the plate counting result on non-selective agar,TSAYE, was used for both target organisms in this study.Cell suspensions of E. coli or L. innocua were inoculatedinto the food items (1:10 w/w) and mixed to give an initialcell count of at least 1.0 · 107 cfu per food item. There wasno dilution of the food items prior to inoculation with themicroorganisms. Before applying the microbial contami-nated food items, all utensils were sterilized. The cheese,eggs, and jelly were pasted on to the ceramic plates, stain-less-steel cutleries (knives, forks and spoons) and plasticserving trays. The quantities of the food items pasted onto the utensils were: plate (5 g), tray (10 g), cutlery(0.5 g). For the glasses, one set was contaminated with0.5 ml of the inoculated milk. In a second set of glasses,0.1 g of lipstick was applied at two locations 180� fromeach other. The lipstick was pasted on to the mouth ofthe glasses while the milk was coated to the inner wall.Contaminated utensils were then exposed to varying wash-ing cycles using a TurboWash II three-compartment man-ual dishwasher manufactured by Hobart Corporation(Troy, OH). Before commencing the washing steps, thefood inoculums on the utensils were air-dried for 1 h at

J. Lee et al. / Journal of Food Engineering 80 (2007) 885–891 887

24 ± 1 �C in an incubator. In order to determine the effectof air drying on the bacteria and to estimate the initialnumber of inoculated organisms on the food contaminatedutensils to be washed, each food type pasted on to a set ofutensils was sampled after air drying. After serial dilutions,bacteria survival numbers were determined by the platecount method.

2.3. Dishwashing process on test utensils

The inoculated utensils were washed in the manual dish-washer. The washer had individual compartments forwashing, rinsing and sanitizing of the ware. Two tempera-ture treatments were used in this study during the washingphase. These were a low temperature (LT) of 24 �C and ahigh temperature (HT) of 43 �C. All utensils were washedwith 100 ppm of Mag Fusion detergent manufactured byEcolab. Inc. (St. Paul, MN), rinsed for 5 s with 24 �Ctap-water, then sanitized in 150 ppm OASIS 146 Multi-Quat sanitizer (manufactured by Ecolab. Inc.) for 5 s. Thisconcentration/time is referred to as a low sanitizing level(LS). The hardness of the tap water was determined usinga Water Quality Test Strip Kit produced by Hach Co.(Loveland, CO). Prior to commencing this study the hard-ness of the rinse water was determined to be 120 mgCaCO3/L. It was essential to determine this value to ensurethat our testing method conformed with the requirementsof the FDA Food Code (2001 b). These codes, 4-501.114(C) and 4-703.11 (C)(3), require quaternary ammoniumcompounds to be used in water with a hardness of notmore than 500 mg CaCO3/L and an exposure time of atleast 30 seconds, respectively. The Food Code also requiresthe quaternary ammonium concentration to be within theguidelines of 21 CFR 178.1010 according to the EPAapproved manufacturer’s label use instructions. For thistest, the strength of the sanitizer recommended by the man-ufacturer was 400 ppm and at a water pH of >6. The pH ofthe water used in this study was determined to be 6.9–7.0.

A second set of utensils were similarly washed andrinsed but were sanitized with 400 ppm of the sanitizerfor 30 s. This concentration is referred to as high sanitizinglevel (HS). The sanitizer was a mixture of four quaternaryammonium compounds (QAC), alkyl dimethyl benzylammonium chloride, alkyl decyl dimethyl ammonium chlo-ride, alkyl didecyl dimethyl ammonium chloride, and alkyldioctyl dimethyl ammonium chloride. Before each test, thedishwasher was thoroughly cleaned using hot steamedwater and refilled with fresh water and detergent/sanitizer.During the washing process, the inoculated utensils wereindividually and manually washed (wearing rubber gloves)using a scrubbing sponge to remove the inoculum (threeclockwise and three anti-clockwise rubs for the dishesand glasses; and three forward and three backward rubsfor the cutleries and trays). The time taken to wash eachutensil was approximately 20 s. All washed utensils wereindividually rinsed in the second compartment of the dish-washer to eliminate the washing water and detach the inoc-

ulated bacteria. After sanitization in the third compartmentof the sink, the utensils were placed in sterilized racks andair-dried for 1 h at 24 �C.

2.4. Microbiological sampling of the utensil surfaces

In the first part of this sampling, hygiene swabs wereused to collect organisms from the surface of ceramicplates, cutleries and glasses that were previously washed.The swabs, made with sterile calcium alginate fiber tipsand wood applicators (Fisher Scientific, Pittsburgh, PA),were moistened before use with a sterile maximum recoverydiluent (MRD) supplied by Oxoid Limited (Basingstoke,UK). These swabs were used to transfer any food/bacteriacombination to test-tubes containing 2 ml of the MRD.These tubes were then vigorously vortexed to release anybacterial cells from the fiber tip of the applicators.

In the second part of the sampling, sponge swab wereused to remove microorganisms from the surface of traysthat were previously washed. This began with stomacherbags containing compressed sterile sponges obtained fromFisher Scientific (Pittsburgh, PA). Each sponge was asepti-cally removed from each bag and moistened with 5 ml ofthe MRD. Using finger pressure, each sponge was pressedthoroughly onto the surface of the trays. Each sponge wasthen returned to the stomacher bag and massaged with45 ml of MRD for 2 min in a Biomaster 80 Stomacher(Seward, London, UK).

2.5. Microbiological and statistical analysis

All cells were serially diluted and plated onto TSAYE todetermine their viable counts after 36 h incubation at37 �C. The detection limit for the test organisms was5 cfu for the trays and 2 cfu for the other utensils. In orderto determine if the bacterial count on the washed samplesresulted from organisms that were inoculated into the food,we simultaneously tested a comparable sample of food thatwas not inoculated with the bacterial species. The presenceof any colonies in the comparable sample after washingwould be evidence of contamination and in such cases,the entire batch of samples would be discarded. No lessthan four sample replicates were used in each experiment.Variances of microbial viability were analyzed by equal-variance t-test using a Microsoft Excel data analysis pro-gram (Ontario, Canada). The level of significance was setfor P < 0.05.

3. Results

3.1. Survival of bacteria in utensils prior to washing

The loss of bacteria from the utensils during the 1 h airdrying step prior to the washing ranged between 0.2 and0.7 log units as seen in Table 1. There were no significantdifferences (P > 0.05) in the reduction of the inoculatedorganisms among the food types pasted on to the utensils.

Table 1Viable counts (log10 cfu per utensil) of bacterial strains in the contaminated foods after air drying at 24 �C for 1 h

Drying Cheese Egg Jelly Lipstick Milk

Plate Cutlery Tray Plate Cutlery Tray Plate Cutlery Tray Wine Regular Wine Regular

Escherichia coli Before 8.5 7.8 9.1 8.9 7.9 9.2 8.8 7.9 9.3 8.2 8.3 7.9 8.1After 8.3 7.6 8.6 8.7 7.7 9.0 8.5 7.6 8.8 7.6 7.7 7.4 7.7

Listeria innocua Before 9.3 8.5 9.5 9.4 8.5 9.5 9.4 8.5 9.7 8.5 8.7 8.2 8.3After 8.8 8.1 9.1 9.0 8.0 9.3 8.9 7.9 9.2 7.8 7.9 7.6 7.8

888 J. Lee et al. / Journal of Food Engineering 80 (2007) 885–891

However, a comparison of the viability for the two organ-isms shows that the desiccation stability of E. coli wasgreater than the desiccation stability of L. innocua. Thisresult is similar to the findings of Bale, Bennett, Beringer,and Hinton (1993) when they reported a greater survivabil-ity of E. coli cells to air drying conditions. This confirmsprevious findings that certain strains of E. coli are more tol-erant to dried condition when compared with other food-borne bacteria.

3.2. Effect of washing conditions on the inactivation of

bacteria in cheese contaminated utensils

Effect of the washing temperature and sanitizer concen-tration on the reduction of E. coli and L. innocua in softcheese on different utensils is shown in Table 2. At low tem-perature (LT) with low sanitizer concentration (LS),approximately 6-log reductions were achieved for L. inno-

cua, whereas E. coli was reduced by 5-logs. When highersanitizing (HS) concentration was applied, the viability ofL. innocua on the plates and knives was significantly(P < 0.05) reduced compared to that of E. coli. Exceptfor bacteria on the forks, the application of HS and hightemperature (HT) reduced the viability of both bacterialtypes on all utensils. However, viable cells were stilldetected even after the application of HT-HS conditionsfor both bacterial types on all utensils.

3.3. Effect of washing conditions on the inactivation ofbacteria in egg contaminated utensils

Compared to cheese, egg on the surface of the utensilswas more easily removed at either low or high washingtemperatures. A microbial count in excess of 6-log reduc-tions was found for both bacterial types after washing atthe combination of LT and LS (Table 2). Except for theforks, the viability of the bacteria was less than 1 log cfuon each utensil at the HT-LS condition. There was no evi-dence of viable cells found on all utensils after washing atthe HT-HS condition, except for L. innocua on the trays.

3.4. Effect of washing conditions on the inactivation of

bacteria in jelly contaminated utensils

The physical removal of jelly during the washing step waseasier when the utensils were washed at HT than at LT. Thereduction in bacterial numbers showed that the LT-LS con-

dition reduced the bacterial survival by more than 6-logunits (Table 2). The number of surviving cells of L. innocua

was lower than that of E. coli after they received higher san-itizing concentration/time (LT-HS), indicating that L. inno-

cua was affected more by the antibacterial activity of thechemicals in the sanitizer. A comparison of the number ofsurviving cells for each bacterial type in washing conditionsLT-LS, LT-HS, and HS-LS showed that E. coli was moreresistant to the sanitization when compare to L. innocua.Among utensils, the survivability of bacteria on the surfaceof forks and plates was higher than that of bacteria on theother utensils at most washing conditions.

3.5. Effect of washing conditions on the inactivation of

bacteria in lipstick contaminated utensils

During this study, it was visually shown that the lipstickpasted on to the mouth of the glasses was more difficult toremove when compare with the other organic matter. Thus,the mouth of most glasses still had lipstick residues afterthe dishwashing process. However, bacterial cells onwashed glasses approximated 8-log reduction after washingat LT-LS (Table 2). Viable cells of both bacterial typeswere not observed on the glasses after all other washingconditions.

3.6. Effect of washing conditions on the inactivation of

bacteria in milk contaminated utensils

Table 2 shows that washing at the LT-LS condition wasnot significant (P > 0.05) to yield a 5-log reduction in bac-terial numbers on the regular glasses. When a higher sani-tizer concentration/time (HS) was applied, reduction in thebacterial numbers on the regular glasses was greater than 6-log units. As can be seen in the results for milk, viable cellswere detected after application of the HT-HS condition forboth bacteria on the regular glasses, whereas no evidence ofviable cells was found on the wine glasses. The results inTable 2 also indicate that, unlike the bacteria in other foodresidues, L. innocua shows better survival when comparedwith E. coli for milk inoculated on to regular glasses atHT-LS and HT-HS conditions.

4. Discussion

The result of this study showed that the viability of bac-terial species contaminating eating utensils can be affected

Table 2Means of viable counts (log10 cfu per utensil) and log reduction of bacterial strains in foods on different utensils washed at varying conditions

Food items Utensils Controla LT-LSb LT-HSc HT-LSd HT-HSe

Escherichia

coli

Listeria

innocua

Escherichia

coli

Listeria

innocua

Escherichia

coli

Listeria

innocua

Escherichia

coli

Listeria

innocua

Escherichia

coli

Listeria

innocua

Rf R R R R R R R

Cheese Plate 8.3 ± 0.1 8.8 ± 0.0 3.1 ± 0.4 5.2 1.9 ± 0.1 6.9 2.5 ± 0.4 5.8 1.1 ± 0.3 7.7 1.3 ± 0.5 7.0 0.8 ± 0.2 8.0 0.3 ± 0.1 8.0 0.4 ± 0.1 8.4Knife 7.6 ± 0.3 8.1 ± 0.2 2.0 ± 0.1 5.6 2.4 ± 0.0 5.7 2.3 ± 0.6 5.3 1.5 ± 0.1 6.6 1.4 ± 0.1 6.2 1.4 ± 0.3 6.7 1.3 ± 0.4 6.3 1.4 ± 0.5 6.7Fork 7.6 ± 0.2 8.2 ± 0.1 2.5 ± 0.1 5.1 2.0 ± 0.1 6.2 2.5 ± 0.3 5.1 2.5 ± 0.3 5.7 2.0 ± 0.0 5.6 2.8 ± 0.2 5.4 1.7 ± 0.8 5.9 2.3 ± 0.2 5.9Spoon 7.7 ± 0.3 8.3 ± 0.3 1.8 ± 0.2 5.9 2.0 ± 0.1 6.3 1.7 ± 0.1 6.0 1.6 ± 0.3 6.7 1.1 ± 0.2 6.6 1.3 ± 0.4 7.0 0.6 ± 0.1 7.1 0.5 ± 0.2 7.8Tray 8.6 ± 0.1 9.1 ± 0.1 3.1 ± 0.4 5.5 2.8 ± 0.1 6.3 2.6 ± 0.2 6.0 2.6 ± 0.2 6.5 1.4 ± 0.1 7.2 1.3 ± 0.1 7.8 1.3 ± 0.2 7.3 1.1 ± 0.5 8.0

Egg Plate 8.7 ± 0.1 9.0 ± 0.1 0.2 ± 0.1 8.5 1.4 ± 0.6 7.6 NDg 0.2 ± 0.2 8.8 ND ND ND NDKnife 7.7 ± 0.0 7.9 ± 0.2 2.5 ± 0.3 5.2 1.1 ± 0.1 6.8 0.2 ± 0.2 7.5 ND 0.8 ± 0.3 6.9 0.4 ± 0.1 7.5 ND NDFork 7.7 ± 0.2 8.0 ± 0.1 1.7 ± 0.4 6.0 1.1 ± 0.2 6.9 0.2 ± 0.1 7.5 0.3 ± 0.3 7.7 1.0 ± 0.2 6.7 0.4 ± 0.1 7.6 ND NDSpoon 7.7 ± 0.0 8.0 ± 0.3 1.4 ± 0.0 6.3 0.9 ± 0.2 7.1 ND ND ND ND ND NDTray 9.0 ± 0.1 9.3 ± 0.2 0.5 ± 0.4 8.5 1.4 ± 0.1 7.9 0.7 ± 0.4 8.3 0.9 ± 0.0 8.4 ND 0.5 ± 0.3 8.8 ND 0.2 ± 0.2 9.1

Jelly Plate 8.5 ± 0.1 8.9 ± 0.1 0.3 ± 0.4 8.2 0.3 ± 0.1 8.6 0.4 ± 0.5 8.1 ND ND 0.6 ± 0.3 8.3 ND 0.1 ± 0.1 8.8Knife 7.6 ± 0.0 7.8 ± 0.2 1.6 ± 0.0 6.0 0.2 ± 0.1 7.6 ND ND 0.3 ± 0.1 7.3 ND ND NDFork 7.6 ± 0.1 7.9 ± 0.1 1.0 ± 0.2 6.6 0.3 ± 0.1 7.6 0.9 ± 0.2 6.7 0.1 ± 0.1 7.8 0.9 ± 0.2 6.7 ND 0.2 ± 0.1 7.4 NDSpoon 7.5 ± 0.2 8.1 ± 0.4 0.6 ± 0.2 6.9 ND ND ND 0.6 ± 0.2 6.9 ND ND NDTray 8.8 ± 0.1 9.2 ± 0.2 2.8 ± 0.0 6.0 1.4 ± 0.4 7.8 1.3 ± 0.2 7.5 ND 0.7 ± 0.1 8.1 ND ND ND

Lipstick Wine glass 7.6 ± 0.1 7.8 ± 0.2 0.2 ± 0.2 7.4 ND ND ND ND ND ND NDRegular glass 7.7 ± 0.3 7.9 ± 0.1 0.3 ± 0.3 7.4 0.1 ± 0.1 7.8 ND ND ND ND ND ND

Milk Wine glass 7.4 ± 0.3 7.6 ± 0.4 1.8 ± 0.3 5.6 1.5 ± 0.2 6.1 0.7 ± 0.4 6.7 0.2 ± 0.1 7.4 ND ND ND NDRegular glass 7.7 ± 0.1 7.8 ± 0.1 2.4 ± 0.3 5.3 3.0 ± 0.2 4.8 1.1 ± 0.2 6.6 0.9 ± 0.2 6.9 0.2 ± 0.1 7.5 0.9 ± 0.4 6.9 0.1 ± 0.1 7.6 0.3 ± 0.2 7.5

a Samples from unwashed condition.b Low sanitizing condition (150 ppm for 5 s) after low washing condition (24 �C).c High sanitizing condition (400 ppm for 30 s) after low washing condition (24 �C).d Low sanitizing condition (150 ppm for 5 s) after high washing condition (43 �C).e High sanitizing condition (400 ppm for 30 s) after high washing condition (43 �C).f Log reduction (R).g No colony was detected on plates from sample replicates (ND).

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890 J. Lee et al. / Journal of Food Engineering 80 (2007) 885–891

by the type of organic matter substrate, the shape of theutensil, the strength of the sanitizing agent and the washingwater temperature. Even though most treatments showedthe ability to produce the 5-log bacterial load reduction,the results showed that some food items such as milk prod-ucts have potential to remain on the utensil and possiblepose a health risk. As a result, we have decided to investi-gate the difficulty in removing milk and milk based prod-ucts and to embark on a long term study of researchaimed at developing more effective methods to removethese types of food products from eating utensils. In worstcase scenarios a 5-log reduction may be hard to achievesince it could be difficult to physically remove some fooditems from certain eating utensils. This can occur if thefood items are allowed to dry on the utensils longer thanthe 1 h period used in this study, for example. The physicalscrubbing action during the wash cycle can also influencethe removal of food particles and thus the presence ofmicroorganisms on eating utensils. In this study we useda scrubbing sponge method for approximately 20 s toremove the inoculum on each utensil. This may varywidely, especially in situations when the need to wash agiven load of utensils may be required in a shorter periodof time. Organic matter, including food residues, is knownto protect bacteria from direct contact with the heat ordetergents used in dishwashing operations (Kusumanin-grum, van Putten, Rombouts, & Beumer, 2002; Lineet al., 1991). Indeed, food residues lodged in dishwasherscan also act as nutrients for bacteria and can cross-contam-inate utensils placed in the washer (Stahl Wernersson,Johansson, & Hakanson, 2004a).

In this study, the highest bacterial load reduction (up to0.8 log unit) occurred when the lipstick was the contami-nating organic matter, even when the mouth of someglasses still had traces of its physical presence. It is possiblethat an antimicrobial agent in the lipstick could have influ-enced this result. The results also showed that bacteriaassociated with milk were more difficult to be removedwhen compared with the other contaminating food items.Other factors influencing the results were the complicatedsurfaces of some utensils, such as the tines on forks andhard-to-reach angled areas of the regular glasses. Thesecan shield the attached organic matter from the rigors ofcleaning.

The findings of this study are supported by variousresearchers who reported on the effectiveness of manualwashing on the elimination of foodborne bacteria such asSalmonella spp., E. coli, Staphylococcus aureus, Campylo-

bacter spp., and Enterococcus faecium (Johansson, StahlWernersson, & Hakanson, 2005; Kusumaningrum et al.,2002; Mattick et al., 2003b; Stahl Wernersson et al.,2004a, 2004b). These reports stated that the bacterial via-bility decreased with increasing air-drying time, washingtemperature, washing time, and the choice of detergent.The degree of tolerance of the bacteria to the above factorsalso depended on their genera and species (Kusumanin-grum et al., 2002; Mattick et al., 2003a).

Table 2 of our results show that E. coli had bettersurvival on the utensils contaminated with jelly, evenwhen high chemical sanitizing concentrations were used.Also, E. coli is known to show some resistance to certainsanitizing agents because of its outer membrane whichcan help to protect the bacterial cell from the action ofthese chemicals (Sundheim, Langsrud, Heir, & Holck,1998). In general, most commercial sanitizers are knownto inactivate Gram-positive bacteria, such as L. innocua

for example, by modifying the cell’s permeability and ini-tiating a subsequent leakage of certain ions in solution.In addition to this, a disruption of ATP synthesis andthe inhibition of membrane-associated enzymatic activi-ties can occur due to an interaction of the sanitizer withthe cytoplasmic membrane of the bacterial cell (Maillard,2002; Weitzel, Pilatus, & Rensing, 1987). With Gram-negative bacteria such as E. coli, on the other hand,detergents can be less effective because of the ability ofthe outer membrane of these organisms to prevent cer-tain chemicals from reaching the cytoplasmic membraneof the cell (Russell, 1992).

This comparison of the bacterial survival under differentwashing conditions in this study allowed us to better under-stand the effectiveness of manual dishwashing for the elim-ination of bacteria from eating utensils. The efficacy of thedishwashing increased with higher concentrations of QACand sanitizing time as well as the higher washing tempera-ture. This information could be used to design washingprotocols that better ensure the sanitization of food contactsurfaces in kitchens, restaurants and food preparationestablishments.

Acknowledgement

The authors wish to thank the Center for InnovativeFood Technology for their financial support for thisproject.

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