Advertisement

Evaluation of bacterial contaminants found on unused paper towels and possible postcontamination after handwashing: A pilot study

  • Louis McCusky Gendron
    Affiliations
    Centre de Recherche de l'Institut Universitaire de Cardiologie et de Pneumologie de Québec, Quebec City, Quebec, Canada

    Département de Biochimie, de Microbiologie et de Bioinformatique, Faculté des Sciences et de Génie, Université Laval, Pavillon Alexandre-Vachon, Quebec City, Quebec, Canada
    Search for articles by this author
  • Luc Trudel
    Affiliations
    Département de Biochimie, de Microbiologie et de Bioinformatique, Faculté des Sciences et de Génie, Université Laval, Pavillon Alexandre-Vachon, Quebec City, Quebec, Canada
    Search for articles by this author
  • Sylvain Moineau
    Affiliations
    Département de Biochimie, de Microbiologie et de Bioinformatique, Faculté des Sciences et de Génie, Université Laval, Pavillon Alexandre-Vachon, Quebec City, Quebec, Canada

    Groupe de Recherche en Ecologie Buccale (GREB) and Félix d'Hérelle Reference Center for Bacterial Viruses, Faculté de Médecine Dentaire, Université Laval, Pavillon de Médecine Dentaire, Quebec City, Quebec, Canada
    Search for articles by this author
  • Caroline Duchaine
    Correspondence
    Address correspondence to Caroline Duchaine, PhD, Centre de recherche, Hôpital Laval, 2725 Chemin Ste-Foy, Ste-Foy (Quebec), G1V 4G5, Canada.
    Affiliations
    Centre de Recherche de l'Institut Universitaire de Cardiologie et de Pneumologie de Québec, Quebec City, Quebec, Canada

    Département de Biochimie, de Microbiologie et de Bioinformatique, Faculté des Sciences et de Génie, Université Laval, Pavillon Alexandre-Vachon, Quebec City, Quebec, Canada
    Search for articles by this author
Published:December 19, 2011DOI:https://doi.org/10.1016/j.ajic.2011.07.007

      Background

      Bacterial contamination is a concern in the pulp and paper industry. Not only is the machinery contaminated but also can be the end-paper products. Bacterial transmission from unused paper towels to hands and surfaces is not well documented.

      Methods

      The culturable bacterial community of 6 different unused paper towel brands was determined by culture methods and by sequencing the 16S ribosomal DNA of bacterial contaminants. Next, we investigated the possible airborne and direct contact transmissions of these bacterial contaminants during hand drying after washing.

      Results

      Between 102 and 105 colony-forming units per gram of unused paper towels were isolated from the different paper towel brands. Bacteria belonging to the Bacillus genus were by far the most abundant microorganisms found (83.0%), followed by Paenibacillus (15.6%), Exiguobacterium (1.6%), and Clostridium (0.01%). Paper towels made from recycled fibers harbored between 100- to 1,000-fold more bacteria than the virgin wood pulp brand. Bacteria were easily transferred to disposable nitrile gloves when drying hands with paper towels. However, no evidence of bacterial airborne transmission was observed during paper towel dispensing.

      Conclusion

      This pilot study demonstrated that a large community of culturable bacteria, including toxin producers, can be isolated from unused paper towels and that they may be transferred to individuals after handwashing. This may have implications in some industrial and clinical settings as well as in immunocompromised individuals.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Infection Control
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Chandra R.
        • Singh S.
        • Krishna Reddy M.M.
        • Patel D.K.
        • Purohit J.H.
        • Kapley A.
        Isolation and characterization of bacterial strains Paenibacillus sp. and Bacillus sp. for kraft lignin decolorization from pulp paper mill waste.
        J Gen Appl Microbiol. 2008; 54: 399-407
        • Desjardins E.
        • Beaulieu C.
        Identification of bacteria contaminating pulp and a paper machine in a Canadian paper mill.
        J Ind Microbiol Biotechnol. 2003; 30: 141-145
        • Namjoshi K.
        • Johnson S.
        • Montello P.
        • Pullman G.S.
        Survey of bacterial populations present in US-produced linerboard with high recycle content.
        J Appl Microbiol. 2010; 108: 416-427
        • Hughes-van-Kregten M.-C.
        Slime flora of New Zealand paper mills.
        Appita. 1988; 41: 470-474
        • Suihko M.-L.
        • Partanen L.
        • Mattila-Sandholm T.
        • Raaska L.
        Occurrence and molecular characterization of cultivable mesophilic and thermophilic obligate anaerobic bacteria isolated from paper mills.
        Syst Appl Microbiol. 2005; 28: 555-561
        • Suihko M.-L.
        • Sinkko H.
        • Partanen L.
        • Mattila-Sandholm T.
        • Salkinoja-Salonen M.
        • Raaska L.
        Description of heterotrophic bacteria occurring in paper mills and paper products.
        J Appl Microbiol. 2004; 97: 1228-1235
        • Suihko M.-L.
        • Skyttä E.
        Characterisation of aerobically grown non-spore-forming bacteria from paper mill pulps containing recycled fibres.
        J Ind Microbiol Biotechnol. 2009; 36: 53-64
        • Suihko M.-L.
        • Stackebrandt E.
        Identification of aerobic mesophilic bacilli isolated from board and paper products containing recycled fibres.
        J Appl Microbiol. 2003; 94: 25-34
        • Öqvist C.K.
        • Kurola J.
        • Pakarinen J.
        • Ekman J.
        • Ikävalko S.
        • Simell J.
        • et al.
        Prokaryotic microbiota of recycled paper mills with low or zero effluent.
        J Ind Microbiol Biotechnol. 2008; 35: 1165-1173
        • Chaudhary A.
        • Gupta L.K.
        • Gupta J.K.
        • Banerjee U.C.
        Studies on slime-forming organisms of a paper mill: slime production and its control.
        J Ind Microbiol Biotechnol. 1997; 18: 348-352
        • Blanco M.A.
        • Negro C.
        • Gaspar I.
        • Tijero J.
        Slime problems in the paper and board industry.
        Appl Microbiol Biotechnol. 1996; 46: 203-208
        • Suominen I.
        • Suihko M.L.
        • Salkinoja-Salonen M.
        Microscopic study of migration of microbes in food-packaging paper and board.
        J Ind Microbiol Biotechnol. 1997; 19: 104-113
        • Vaisanen O.M.
        • Mentu J.
        • Salkinoja-Salonen M.S.
        Bacteria in food packaging paper and board.
        J Appl Bacteriol. 1991; 71: 130-133
        • Russell A.D.
        Bacterial spores and chemical sporicidal agents.
        Clin Microbiol Rev. 1990; 3: 99-119
        • Suihko M.L.
        • Skytta E.
        A study of the microflora of some recycled fibre pulps, boards and kitchen rolls.
        J Appl Microbiol. 1997; 83: 199-207
        • Oppong D.
        • King M.V.
        • Bowen A.J.
        Isolation and characterization of filamentous bacteria from paper mill slimes.
        Int Biodeterioration Biodegrad. 2003; 52: 53-62
        • Vaisanen O.M.
        • Nurmiaho-Lassila E.-L.
        • Marmo S.A.
        • Salkinoja-Salonen M.S.
        Structure and composition of biological slimes on paper and board machines.
        Appl Environ Microbiol. 1994; 60: 641-653
        • Marchesi J.R.
        • Sato T.
        • Weightman A.J.
        • Martin T.A.
        • Fry J.C.
        • Hiom S.J.
        • et al.
        Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA.
        Appl Environ Microbiol. 1998; 64: 795-799
        • Gilbert Y.
        • Veillette M.
        • Duchaine C.
        Metalworking fluids biodiversity characterization.
        J Appl Microbiol. 2009; 108: 437-449
        • Yamamoto Y.
        • Ugai K.
        • Takahashi Y.
        Efficiency of hand drying for removing bacteria from washed hands: comparison of paper towel drying with warm air drying.
        Infect Control Hosp Epidemiol. 2005; 26: 316-320
        • Andersen A.A.
        New Sampler for the collection, sizing, and enumeration of viable airborne particles.
        J Bacteriol. 1958; 76: 471-484
        • Sorrelle P.
        • Belgard W.
        The effect of recycled fiber use on paper machine biological control. TAPPI Paper makers Conference.
        TAPPI Press, Atlanta [GA]1991 (p. 569-75)
        • Sorrelle P.
        • Belgard W.
        Growth in recycling escalates costs for paper machine biological control.
        Pulp Pap. 1992; : 57-64
        • Johansson A.
        • Hallmans G.
        • Holm S.E.
        • Olofsson C.
        • Gref R.
        • Svensson K.
        • et al.
        Microflora in paperboard with various contents of recycled fibers.
        Nord Pulp Paper Res J. 2001; 16: 40-45
        • Robertson L.
        Microhial growth in starch.
        PIMA Mag. 1994; 76: 74-76
        • Majcher M.R.
        • Bernard K.A.
        • Sattar S.A.
        Identification by quantitative carrier test of surrogate spore-forming bacteria to assess sporicidal chemicals for use against Bacillus anthracis.
        Appl Environ Microbiol. 2008; 74: 676-681
        • Conkey J.H.
        Sporicidal activities of chlorine, chlorine dioxide, and peracetic acid in a simulated papermaking furnish.
        TAPPI. 1981; 64: 101
        • Hong H.A.
        • To E.
        • Fakhry S.
        • Baccigalupi L.
        • Ricca E.
        • Cutting S.M.
        Defining the natural habitat of Bacillus spore formers.
        Res Microbiol. 2009; 160: 375-379
        • Nicholson W.L.
        Roles of Bacillus endospores in the environment.
        Cell Mol Life Sci. 2002; 59: 410-416
        • Claus D.
        • Berkeley R.C.W.
        Genus Bacillus Cohn 1872, 174.
        in: Sneath P.H.A. Mair N.S. Sharpe M.E. Holt J.G. Bergey's manual of systematic bacteriology. Vol. 2. Williams & Wilkins, Baltimore [MD]1986: 1105-1139
        • Robinton E.D.
        • Mood E.W.
        A study of bacterial contaminants of cloth and paper towels.
        Am J Public Health Nations Health. 1968; 58: 1452-1459
        • Ash C.
        • Priest F.G.
        • Collins M.D.
        Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test.
        Antonie Van Leeuwenhoek. 1993; 64: 253-260
        • Dutil S.
        • Mériaux A.
        • de Latrémoille M.-C.
        • Lazure L.
        • Barbeau J.
        • Duchaine C.
        Measurement of airborne bacteria and endotoxin generated during dental cleaning.
        J Occup Environ Hyg. 2009; 6: 121-130
        • Gilbert Y.
        • Veillette M.
        Airborne bacteria and antibiotic resistance genes in hospital rooms.
        Aerobiologia. 2010; 26: 185-194
        • Létourneau V.
        • Nehmé B.
        • Mériaux A.
        • Massé D.
        • Duchaine C.
        Impact of production systems on swine confinement buildings bioaerosols.
        J Occup Environ Hyg. 2010; 7: 94-102
        • Oppong D.
        • King V.M.
        • Zhou X.
        • Bowen J.A.
        Cultural and biochemical diversity of pink-pigmented bacteria isolated from paper mill slimes.
        J Ind Microbiol Biotechnol. 2000; 25: 74-80
        • Vieira F.C.
        • Nahas E.
        Comparison of microbial numbers in soils by using various culture media and temperatures.
        Microbiol Res. 2005; 160: 197-202
        • Andersson A.
        • Ronner U.
        • Granum P.E.
        What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens?.
        Int J Food Microbiol. 1995; 28: 145-155
        • Priha O.
        • Hallamaa K.
        • Saarela M.
        • Raaska L.
        Detection of Bacillus cereus group bacteria from cardboard and paper with real-time PCR.
        J Ind Microbiol Biotechnol. 2004; 31: 161-169
        • Hoornstra D.
        • Dahlman O.
        • Jääskeläinen E.
        • Andersson M.A.
        • Weber A.
        • Aurela B.
        • et al.
        Retention of Bacillus cereus and its toxin, cereulide, in cellulosic fibres.
        Holzforschung. 2006; 60: 648-652
        • Bottone E.J.
        Bacillus cereus, a volatile human pathogen.
        Clin Microbiol Rev. 2010; 23: 382-398
        • Beattie S.H.
        • Williams A.G.
        Detection of toxigenic strains of Bacillus cereus and other Bacillus spp. with an improved cytotoxicity assay.
        Lett Appl Microbiol. 1999; 28: 221-225
        • Phelps R.J.
        • McKillip J.L.
        Enterotoxin production in natural isolates of Bacillaceae outside the Bacillus cereus group.
        Appl Environ Microbiol. 2002; 68: 3147-3151
        • Matsumoto S.
        • Suenaga H.
        • Naito K.
        • Sawazaki M.
        • Hiramatsu T.
        • Agata N.
        Management of suspected nosocomial infection: an audit of 19 hospitalized patients with septicemia caused by Bacillus species.
        Jpn J Infect Dis. 2000; 53: 196-202
        • Krause A.
        • Gould F.K.
        • Forty J.
        Prosthetic heart valve endocarditis caused by Bacillus circulans.
        J Infect. 1999; 39: 160-162
        • De Jonghe V.
        • Coorevits A.
        • De Block J.
        • Van Coillie E.
        • Grijspeerdt K.
        • Herman L.
        • et al.
        Toxinogenic and spoilage potential of aerobic spore-formers isolated from raw milk.
        Int J Food Microbiol. 2010; 136: 318-325
        • Rusin P.
        • Maxwell S.
        • Gerba C.
        Comparative surface-to-hand and fingertip-to-mouth transfer efficiency of gram-positive bacteria, gram-negative bacteria, and phage.
        J Appl Microbiol. 2002; 93: 585-592
        • Harrison W.A.
        • Griffith C.J.
        • Ayers T.
        • Michaels B.
        Bacterial transfer and cross-contamination potential associated with paper-towel dispensing.
        Am J Infect Control. 2003; 31: 387-391
        • Gustafson D.R.
        • Vetter E.A.
        • Larson D.R.
        • Ilstrup D.M.
        • Maker M.D.
        • Thompson R.L.
        • et al.
        Effects of 4 hand-drying methods for removing bacteria from washed hands: a randomized trial.
        Mayo Clinic Proc. 2000; 75: 705-708
        • Ansari S.A.
        • Springthorpe V.S.
        • Sattar S.A.
        • Tostowaryk W.
        • Wells G.A.
        Comparison of cloth, paper, and warm air drying in eliminating viruses and bacteria from washed hands.
        Am J Infect Control. 1991; 19: 243-249
        • Matthews J.A.
        • Newsom S.W.
        Hot air electric hand driers compared with paper towels for potential spread of airborne bacteria.
        J Hosp Infect. 1987; 9: 85-88