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Journalof Food Protection, Vol. 65, No. 1, 2002, Pages 61– 65 Copyright Q,InternationalAssociation for FoodProtection

Effects ofAntibacterial DishwashingLiquid on Foodborne Pathogensand Competitive Microorganisms inKitchen Sponges

H.D.KUSUMANINGRUM, M.M. VAN PUTTEN, F. M.ROMBOUTS, AND R. R. BEUMER*

Laboratoryof FoodMicrobiology, Department of Agrotechnology and Food Sciences, WageningenUniversity, P.O.Box 8129, 6700 EV Wageningen, TheNetherlands

MS01-154:Received 19April 2001/ Accepted 10August 2001 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/65/1/61/1675017/0362-028x-65_1_61.pdf by guest on 29 September 2021 ABSTRACT

Inresponse to increasing concern about home hygiene, the use of antibacterial products to reduce microorganisms in kitchensponges and cleaning cloths is strongly promoted by some producers of detergent for domestic use. The effects of an antibacterialdishwashing liquid on Escherichiacoli, Salmonella Enteritidis, Staphylococcusaureus, and Bacilluscereus were investigatedin a modiŽed suspension test and in used sponges with and without food residues under laborator yconditions. Alimitedstudy was conducted in householdsto assessthe efŽ cacy of antibacterialdishwashing liquid as used by the consumer . Inthe suspension tests, S. aureus and B. cereus wereshown to be susceptibleto low concentrations of antibacterialdishwashing liquid(0.5%), whereas E. coli and Salmonella Enteritidismaintained their initial numbers for at least24 hat25 8C. At higher concentrations(2 to 4%), all test organisms decreased to below the detection limit after 24 h. Over a 24-hperiod, the antibacterialdishwashing liquid did not signiŽ cantly reduce these organisms in used sponges in which food residues were present.The antibacterial product did not reduce the competitive microorganisms either. Similar results were found for sponges involvedin daily household use. The results of this study demonstrate that the antibacterial dishwashing liquid was effective inreducing pathogens in the suspension test but not in the used sponges. This Ž ndingindicates that to determine the efŽ cacy ofantibacterial products, their use in a householdsetting must be considered.

Previousstudies have caused increasing concern about cacyas adecontaminatingagent (2). Aproduct’s effective- foodbornedisease outbreaks in thehome setting. These out- nessin reducing microorganisms also depends on the way breakshave frequently occurred as a resultof improper theproduct is applied by the consumer (3), because the foodpreparation (1,10, 13, 17), andcross-contamination consumerdoes not always use the product as directed by incombinationwith inadequate storage or cookinghas been themanufacturer . implicatedin many instances (1, 10). Theseprevious stud- Inthis study, the effects of anantibacterial dishwashing ieshave suggested that although raw materialis probably liquidon foodborne pathogens were investigatedin amod- themain source of contamination in the kitchen, the areas iŽed suspension test and in used sponges with and without surroundingthe kitchen could also act as sources of free- foodresidues under laboratory conditions. The efŽ cacy of livingpopulations of bacteria.Dishcloths and sponges have theantibacterial version of thisproduct in comparisonwith beenrecognized as potential agents in thespread of micro- thatof theregular version was studiedunder the conditions organisms,and it hasbeen observed that bacteria persist in ofpractical use in a limitednumber of households. thesevehicles (9,12, 16, 18). Entericpathogens such as Escherichiacoli, Klebsiella pneumoniae, and Enterobacter MATERIALS AND METHODS cloacae havebeen isolated, as have other types of patho- Spongesand dishwashingliquid. Syntheticyellow sponges gens (Staphylococcusaureus, )andopportunistic pathogens withgreen pads (Lola, 9 by7 by3 cm;Nedac, Duiven, The (Pseudomonas spp.) (5, 16, 18). Netherlands)and dishwashing liquids (antibacterial product and Manyantibacterial products are speciŽ cally manufac- regularproduct) were obtained from retail supermarkets. Used turedfor thereduction of bacteria in cleaning cloths and spongeswere collected from earlier laboratory experiments on the sponges.These products include bleach solutions, deter- survivalof pathogens in new sponges (unpublished), washed with gents,and dishwashing liquids. Limited studies have ad- 0.05%dishwashing liquid in hot water (60 to 65 8C),air dried, dressedthe effectiveness of these products in inactivating andstored at room temperature for 1 to2 weeks. microorganismson sponges.In previous studies, it hasbeen reportedthat the soaking of dishclothsor spongesfor 5min Testmicroorganisms. Fourstrains from our culture collec- inbleach solution resulted in a .99.9%reduction of mi- tionwere used: E. coli Ec-0025(minced meat isolate, obtained croorganisms (7, 15). However,thepresence of food sub- fromthe Inspectorate for Health Protection, The Netherlands), Salmonella EnteritidisSa-0046 (PT4, chicken product isolate), stancesor other matter likely decreases this product’ s efŽ- Staphylococcusaureus Sc-0010(human isolate, enterotoxin A producer),and Bacilluscereus Ba-0001(environmental isolate *Authorfor correspondence. T el: 131(317) 48 3213; Fax: 1031 (317) froma dairyprocessing plant). From overnight cultures (20 to 24 4849 78; E-mail: [email protected]. h)inbrainheart infusion (BHI) broth (Difco Laboratories, Detroit, 62 KUSUMANINGRUM ETAL. J.FoodProt., Vol. 65, No. 1

FIGURE 1. Effectof antibacterial dish- washingliquid on pathogens in the modi- Žedsuspension test. Percentages indicate theconcentrations of dishwashing liquid; timezero represents the number of thetest organismsimmediately after contamina- tion. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/65/1/61/1675017/0362-028x-65_1_61.pdf by guest on 29 September 2021

Mich;Becton Dickinson and Co., Paramus, N.J.), 0.75 ml of sus- reus, incubatedfor 18 to 40 h at30 8C.Platecount agar (Oxoid) pensionwas added to cryo vials containing 0.25 ml glycerol and wasused for total aerobic counts and was incubated for 24 to48 2-mm-diameterglass beads and stored at 2208C.Theywere ac- h at 308C.ForidentiŽ cation of bacteria, Analytab Products kits tivatedby the transfer of one bead to 10 ml of BHI suspension, (20E,20NE, API Staph,and 50 CHB; BioMe´reux,France) were followedby incubationfor 20 to 24 hat37 8C for E. coli Ec-0025, used. Salmonella EnteritidisSa-0046, and S. aureus Sc-0010and at 308C for B. cereus Ba-0001. Practical-usestudy. Ineight households, the antibacterial dishwashingliquid, packed in a sterileplastic jar ,wasapplied to Suspension test. Overnightcultures in BHI brothwere di- spongesaccording to the manufacturer’ s instructionsand used dai- lutedin saline solution (0.85% NaCl) and added to various con- lyfor a 2-weekperiod. Its effect on the reduction of microorgan- centrationsof the antibacterial dishwashing liquid in saline solu- ismswas compared with that of theregular product, examined at 4 tion(0, 0.5, 1, 2, and 4%) to Ž nalconcentrations of about 10 thesame households for another 2-week period. Microbiological CFU/ml.Enumeration of the test strains was performed directly investigationsof the sponges for total aerobic counts, coliforms, aftercontamination and after 6 and24 h ofcontact time at 25 8C. andpseudomonads were performed on days 3, 7,and14 by sam- Effectof antibacterial dishwashing liquid in laboratory plingas described above. The coliforms were enumerated on sponges. Theused sponges were washed with antibacterial dish- Chromocultcoliform agar and incubated for 24 hat37 8C, and the washingliquid solution (0.05%) in warm water (40 to 45 8C) in a pseudomonadswere enumerated on pseudomonas agar (Oxoid) sinkto simulate daily dishwashing and were treated with a squirt andincubated at 30 8C for 48 h. ofdishwashing liquid as described in the manufacturer’ s instruc- tions,resulting in 0.5 6 0.2g persponge (3% 6 1.5%,wt/ wt). Statisticalanalyses. Threereplications were performed for Sixsponges were each contaminated with 10 ml of testsus- suspensiontests, and two were performed for laboratory sponges. pensionand squeezed with gloved hands to distributethe suspen- Student’s two-tailedpaired t testwas used to analyze the signiŽ - sionin the sponges. The test suspensions were prepared by dilut- canceof the difference in the levels of thetest organisms in used ingovernight cultures in BHI brothin saline solution and 10% spongesat contamination and after 24 h. A one-wayfactorial anal- commercialsterilized milk in saline solution to approximately10 6 ysisof variancewas used for the other experiments. A P value of CFU/ml.In order to generate soiled conditions, the cultures were ,0.05was considered statistically signiŽ cant. alsodiluted in 1% lettuce suspension in saline solution and 0.1% suspensionof raw chicken breast Ž lletin saline solution. RESULTS Spongeswere stored at room temperature (20 to 25 8C, 42% Suspension test. Alltest organisms demonstrated rapid 6 2%relative humidity) and sampled on various days (days 0, 1, growthin BHI broth(control) and a slowincrease in num- 2,4, 7, and 10) by suspending the whole sponge in 100 ml of sterilepeptone saline solution (0.1% peptone) with a Stomacher berin saline solution (blank), as shown in Figure 1. Im- laboratoryblender (Seward, UK) for60 s. mediatelyafter exposure to 0.5% antibacterial dishwashing liquidin saline solution, the numbers of B. cereus were Enumerationof testmicroorganisms. Appropriatedilutions belowthe detection limit (log cell numbers [ N] # 1.3), and werespread with a spiralplater (Eddy Jet, IUC) on selectiveme- a .90%reduction of S. aureus was obtained. E. coli and dia:Chromocult coliform agar (Merck, Darmstadt, Germany) for Salmonella Enteritidismaintained their initial numbers for E. coli, incubatedfor 24 h at37 8C;Mannitollysine crystal violet brilliantgreen agar (Oxoid) for Salmonella Enteritidis,incubated atleast 24 hinthepresence of 0.5%of the product, whereas for18 of 24 h at37 8C;BairdParker egg yolk– tellurite agar (Ox- witha 1%concentration only a smallreduction was ob- oid,Basingstoke, UK) for S. aureus, incubatedfor 24 to 48 h at served.With higher concentrations (2 to 4%), all test or- 378C;andMannitol egg yolk polymixine agar (Merck) for B. ce- ganismswere belowthe detection limit after 24 h; for S. J.FoodProt., Vol. 65, No. 1 EFFECTSOF DISHWASHING LIQUID ONPATHOGENS 63

FIGURE 2. Effectof antibacterial dish- washingliquid on pathogens in artiŽcially usedsponges (A) contaminated with test organismsin saline solution suspension and(B) contaminatedwith test organisms in10% milk-saline solution suspension. Symbols: m,directlyafter contamination; M, after 24 h.

aureus and B. cereus, thenumbers decreased immediately Figure3 showsthe effect of the antibacterial dish-

afterthe test inoculum was added. washingliquid on the test organisms and the competitive Downloaded from http://meridian.allenpress.com/jfp/article-pdf/65/1/61/1675017/0362-028x-65_1_61.pdf by guest on 29 September 2021 microora in used laboratory sponges for aperiodof 10 Effect ofantibacterial dishwashing liquid in labo- days,during which the water content of the sponges de- ratorysponges. Inuncontaminated used laboratory spong- clinedfrom 80%to 7%(wt/wt). Withoutfood residues (Fig. es,the pathogens speciŽ ed in this study were notfound, 3A,3C, 3E, and 3G), thetest organisms decreased in num- 5 6 andthe total aerobic counts were about10 to 10 CFU per ber,withthe exception of B. cereus, whichsurvived and sponge(data not shown). maintainedits initial number .Thetotal aerobic counts dem- Withthe amount of dishwashing liquid added to the onstratedsubstantial increases for 48h (1to 3 logunits). sponges (3% 6 1.5% w/w), E. coli increasedin number Withadditional milk substances (4%, vol/ wt), thetotal aer- during24 h bothwith and without food residues, whereas obiccounts and the number of E. coli increasedwith a log theother test organisms decreased by ,2logunits (Fig. factorof 2 to3 for 48h. Thereafter ,theirnumbers de- 2).The paired Student’ s t testdemonstrated no statistical creasedto the initial level (approximately 10 6 CFU per signiŽcance between the levels of all test organisms in sponge).Only S. aureus demonstrateda signiŽcant de- spongesat contamination and after 24 hofstorageat room crease,of 3 logunits. The levels of Salmonella Enteritidis temperature,with the exception of Salmonella Enteritidis and B. cereus (approximately10 6 CFUpersponge) did not and S. aureus withoutfood residues. changeconsiderably during the test period (10 days).

FIGURE 3. Effectof antibacterial dish- washingliquid on the survival of patho- gensand their competitive micro ora (to- talaerobic counts) in used sponges artiŽ - ciallycontaminated with (A) E. coli in sa- linesolution and in 10% milk-sali ne solutionsuspension, (B) E. coli in lettuce andchicken Ž lletsuspension, (C) Salmo- nella Enteritidisin saline solution and in 10%milk-saline solution suspension, (D) Salmonella Enteritidisin lettuce and chick- enŽlletsuspension, (E) S. aureus in saline solutionand in 10% milk-saline solution suspension,(F) S. aureus inlettuce and chickenŽ lletsuspension, (G) B. cereus in salinesolution and in 10% milk-saline so- lutionsuspension, and (H) B. cereus in let- tuceand chicken Ž lletsuspension. 64 KUSUMANINGRUM ETAL. J.FoodProt., Vol. 65, No. 1

FIGURE 4. Effectof (A) antibacterial dishwashingliquid and (B) regular dish- washingliquid on micro ora in household sponges. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/65/1/61/1675017/0362-028x-65_1_61.pdf by guest on 29 September 2021

Inthe presence of lettuceand chicken breast Ž lletsus- theproduct can reduce cross-contamination under condi- pension(Fig. 3B, 3D, 3F ,and3H), S.aureus,B. cereus, tionsof actual household use. andthe total aerobic counts showed results similar to those Becausethe outcome of suspension tests might be a foundin the presence of milk substances. E. coli and Sal- poorpredictor of efŽ cacy under practical conditions, es- monella Enteritidissurvived better in thesesponges than in peciallywith regard to bacteria attached to surfaces and in spongeswithout food residues but not as well as they did thepresence of food debris, a varietyof test procedures inthe presence of milk substances. havebeen designed to mimic these conditions (20). There AnalytabProducts identiŽ cation of colonies isolated aremany variants of the test whereby distribution of the from platecount agar plates showed that the predominant disinfectantsolution over a smalldeŽ ned test surface (tile, microorganismswere Pseudomonasputida (55%) and microscopicslide, PVC, stainlesssteel disk) is followed by Pseudomonas uorescens (23%).In Chromocult plates, E. contaminationwith a standardizedinoculum and determi- cloacae was themost frequently isolated bacterium (60%). nationof the survivors after a givenexposure time by a Thesemicroorganisms were foundin all sponges. rinsingtechnique (11). Practical-usestudy. Thesponges involved in daily use Inthis study, some modiŽ cations were madeto the inhouseholds were incontact with the dishwashing liquid standardsuspension tests to simulate practical conditions. atleast once a day.The total aerobic counts during the test Therefore,the level of artiŽ cial contamination was rela- 4 periodof 14days(approximately 10 6 CFUpersponge) did tivelylow (approximately 10 CFU/ml),and the tested con- notchange dramatically (Fig. 4) when either the antibac- centrationsof theproduct were ina rangeof dilutionsthat terialproduct or the regular product was used.Daily ap- aregenerally applied in a householdsituation: 0.1% 6 plicationof the antibacterial dishwashing liquid to the 0.05%in water for dishwashingand 3% 6 1.5% for ap- spongeshad only a slighteffect on the numbers of coli- plicationto sponges.The effect of antibacterial dishwashing forms andpseudomonads. There was noclear indication liquidin used sponges was studiedfor arelativelylong thatone of thesegroups became the predominant micro ora period(10 days under laboratory conditions and 14 days inthe sponges during the 2-week examination. underpractical conditions) to include the possible changes Inonly one of eight households did analysis of variance incomposition of the micro ora in the sponges. demonstratesigniŽ cant differences ( P , 0.05)between the Inthe suspension test, S. aureus and B. cereus were levelsof microorganisms (less than log factor 2) in the shownto be more susceptible to the antibacterial product spongeswith the antibacterial product and with the regular than were E. coli and Salmonella Enteritidisat lowconcen- product.This Ž ndingsuggests that the effect of dailyappli- trations(0.5%). This result might be dueto the tolerance of cationof this antibacterial product by the consumer is not thesebacteria to theantibacterial compounds in the product. reallydifferent from theeffect of thatof the regular product. Gram-positivebacteria are generally sensitive to membrane- activedisinfectants (19). Anionicsurfactants that are includ- DISCUSSION edin the composition of the product in a relativelyhigh Antibacteriald ishwashingliq uid,whichfor some concentration(15 to 30%) might contribute to the inactiva- brandsis distinguished from aregularproduct by the ad- tionof gram-positivebacteria, because these compounds, as ditionof oneor moreantibacterial compounds, is supposed typicaltargets, affect cytoplasmic membrane integrity and toreduce or inactivatebacteria. The efŽ cacy of suchprod- membrane-boundenzymes and cause cell leakage (4, 19). uctsis usually tested under laboratory conditions using sus- Increasingthe concentration of the antibacterial prod- pensiontests in whicha generallyaccepted requirement for uct(2 to 4%), which in thesuspension tests reduced all test disinfectantsis a logreduction of $5(a reductionof organismsto below the detection limit after 24 h, did not $99.999%)during 5 minof contact (11). Someof these resultin a considerableeffect for thesponges used under productsare able to meet the test requirements, but there laboratoryconditions. The numbers of E.coli,Salmonella islittleevidence with regard to whether and to whatextent Enteritidis,and B. cereus andtotal aerobic counts were J.FoodProt., Vol. 65, No. 1 EFFECTSOF DISHWASHING LIQUID ONPATHOGENS 65 hardlyin uenced by the antibacterial activity of the prod- Salmonella Enteritidis,and B. cereus andtotal aerobic uct,particularly if foodresidues were present.The cavern- countswere hardlyin uenced. The presence of food resi- ousstructure of thesponge might offer aprotectivemicro- duesstrongly reduces the product’ s efŽcacy. This Ž nding environmentin which microbial attachment and survival is indicatesthat to determine the efŽ cacy of an antibacterial facilitated (6). Inthis structure, food residues left after dish- productand other similar products, practical conditions washingmight form abioŽlm that inactivates the antibac- mustbe considered in the test. terialcompounds (2, 4, 11). 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