Rechargeable Antimicrobial Surface Modification of Polyethylene

2042

Journal of Food Protection, Vol. 71, No. 10, 2008, Pages 2042–2047 Copyright ᮊ, International Association for Food Protection

Rechargeable Antimicrobial Surface Modiﬁcation of Polyethylene

J. M. GODDARD AND J. H. HOTCHKISS*

Department of Food Science, Cornell University, Stocking Hall, Ithaca, New York 14853, USA

MS 08-041: Received 22 January 2008/Accepted 17 May 2008

ABSTRACT Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/10/2042/2204454/0362-028x-71_10_2042.pdf by guest on 02 October 2021

Polyethylene films were surface modified, to incorporate amine and amide functionalities, and subsequently were evaluated for their ability to recharge the antimicrobial N-halamine structures after contact with sodium hypochlorite, a common food- approved sanitizer. Surfaces were tested for chlorine retention and release, as well as antimicrobial activity against microorganisms relevant to food quality and food safety, including Escherichia coli K-12, Pseudomonas fluorescens, Bacillus cereus, and Listeria monocytogenes. N-Halamine functionalized polyethylene exhibited chlorine rechargeability, maintaining 5 to 7 nmol/cm2 N-halamine structures for six successive charges. The N-halamine functionalized films achieved a 4-log reduction for all organisms tested and maintained a greater than 3-log reduction for four successive uses, suggesting that the modified polyethylene films are capable of providing rechargeable antimicrobial activity. The modified films exhibited antimicrobial activity in aqueous suspensions (P Ͻ 0.05) and reduced microbial growth in diluted broth (P Ͻ 0.05), suggesting the potential for biocidal action even in the presence of organic matter. Such a rechargeable antimicrobial surface could supplement existing cleaning and sanitation programs in food processing environments to reduce the adhesion, growth, and subsequent cross- contamination of food pathogens, as well as food spoilage organisms.

Foodborne diseases are estimated to cause 76 million which is then free to inactivate microorganisms (38). Al- illnesses annually (28). In addition to the public health con- ternatively, the intact N-halamine might inactivate micro- cern, the financial effect of product recalls (7) and the re- organisms by direct oxidation of biomolecules within the sulting drop in consumer confidence must be taken into microorganism (DNA, RNA, lipids, proteins) (13, 27). The account. Microbial growth also results in economic losses imides, amides, or amines can then be recharged with com- from spoilage (25). Surfaces such as filler nozzles, gasket mercial bleach (sodium hypochlorite) to regain its antimi- materials, conveyor belts, and work tables are prime loca- crobial chlorinated structure. This cycle can be repeated a tions for bacterial adhesion and subsequent contamination number of times. of product. If the food contact surface to which bacteria Textiles and nonwoven fabrics capable of reversibly have adhered were self-sanitizing, it could enhance current and repeatedly forming N-halamine structures have been cleaning and sanitization protocols by providing sustained investigated, as well as polystyrene beads and coatings suit- antimicrobial activity. able for pools and water disinfection applications (3, 5, 8, Commercial antimicrobial surfaces such as AgION 9, 26, 31–37). Similar materials might be applicable in the (AgION Technologies, Inc., Wakefield, Mass.) and Micro- food industry because processing surfaces could become ban (Microban International, Ltd., New York, N.Y.), with recharged after treatment with sodium hypochlorite, a com- silver zeolite and triclosan as the respective active agents, mon approved food contact sanitizing agent (13, 27). Dur- require migration from the surface to be effective. Thus, ing the subsequent processing run, the chlorine could in- the antimicrobial activity of the surface decreases over time activate microorganisms, providing a surface that resists (2, 11, 12). In addition to limited lifetime because of dif- colonization, multiplication, and cross-contamination of fusion of the active compound, silver zeolite– and triclosan- food pathogens and food spoilage organisms. incorporated surfaces have the risk of promoting the de- We have previously developed methodologies for mod- velopment of antimicrobial-resistant organisms (6, 15, 20, ifying the surface chemistry of polyethylene and other 22, 23) and might not be effective in a food-processing polymer surfaces (18, 19). One such surface-modified poly- environment (24, 30). In recent years, a new strategy has ethylene, PE-polyCOOH, was developed by covalently im- been investigated—rechargeable antimicrobial activity. mobilizing polyacrylic acid to oxidized polyethylene via a Chlorination of the nitrogens in imides, amides, and amines polyethylenimine linkage. The hypothesis of this work was results in formation of N-halamine structures (1, 10). In an that the numerous amides and amines present on the surface aqueous environment, N-halamines dissociate to release of PE-polyCOOH films would reversibly charge with chlo- free chlorine (hypochlorous acid and hypochlorite ion), rine, and that chlorine-charged PE-polyCOOH films would possess antimicrobial activity. The specific objectives were * Author for correspondence. Tel: (607) 255-7900; Fax: (607) 254-4868; to assess the chlorine rechargeability of PE-polyCOOH E-mail: [email protected]. films and to evaluate the antimicrobial activity of chlorine- J. Food Prot., Vol. 71, No. 10 RECHARGEABLE ANTIMICROBIAL POLYETHYLENE 2043

FIGURE 1. Structure and chlorination of PE-polyCOOH films. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/10/2042/2204454/0362-028x-71_10_2042.pdf by guest on 02 October 2021 charged PE-polyCOOH films against a range of microor- which was prepared by soaking glassware in a 100 ppm of NaOCl ganisms relevant in food safety and food spoilage. aqueous solution for 1 h, followed by rinsing in copious water. The amount of chlorine available from the PE-polyCOOH-Cl MATERIALS AND METHODS films was determined by a modification of the DPD assay. DPD reagent was prepared by dissolving one packet of DPD total chlo- Additive free, low-density polyethylene 640I (PE, 100 ␮m) rine reagent powder in 1 ml of reagent-grade deionized water. was kindly donated by Dow Chemical Company (Midland, Films were submerged in 2 ml of reagent-grade deionized water Mich.). Polyacrylic acid (molecular weight [MW], 450,000) was to which 50 ␮l of the DPD reagent was added. After 2 min of purchased from Scientific Polymer Products (Ontario, N.Y.). Chro- shaking at room temperature, absorbances were read at 512 nm, mium trioxide (anhydrous), sodium hypochlorite (5%), N,N-dieth- and the concentration of free chlorine was determined by com- yl-p-phenylenediamine (DPD) total chlorine reagent, and toluidine parison to a standard curve of sodium hypochlorite in reagent- blue O were purchased from Fisher Scientific (Fair Lawn, N.J.). grade deionized water. PE, PE-COOH, and PE-polyNH films sub- Acid orange 7, 1-ethyl-3-(3-dimethylamino-propyl) carbodiimide, 2 jected to chlorine charging (15 min of shaking in 3,000 ppm of and N-hydroxysuccinimide (NHS) were purchased from Sigma- NaOCl), as well as unchlorinated films at each step of modifica- Aldrich (St. Louis, Mo.). Reagent-grade deionized water was pur- tion, served as controls. chased from RICCA Chemical Company (Arlington, Tex.). Foam Force LP, an alkaline NaOCl-based cleaner used in dairy saniti- Antimicrobial activity of chlorinated polyethylene. To zation, was purchased from Ecolab, Inc. (St. Paul, Minn.). All grow pure cultures, isolates were streaked onto TSA plates and other reagents were obtained from commercial lab supply stores incubated at 30 or 37ЊC for 24 to 48 h until isolated colonies and were reagent grade or better. appeared. TSB was inoculated with a single colony and incubated Escherichia coli K-12 (ATCC 29425) was obtained from the overnight at 30 or 37ЊC with shaking. Overnight cultures were American Type Culture Collection (Manassas, Va.). All other iso- adjusted to 1 to 5 ϫ 108 CFU/ml to match McFarland Standard lates were obtained from the Cornell University Food Science 0.5 to 1 (Remel, Lenexa, Kans.). Of the 1 ϫ 108 to 5 ϫ 108 CFU/ Food Safety Laboratory culture collection, where they were stored ml culture, 250 ␮l was added to 25 ml of diluent to reach a final Ϫ Њ at 80 C until use. Pseudomonas fluorescens (FSL D3-283) was concentration of 106 to 107 CFU/ml. Two sterile diluents (water isolated from the valve of a dairy plant (14); Listeria monocyto- or 10% TSB) were tested to assess the effectiveness of the films genes (FSL F2-944) was isolated from a swab of a meat cutting in different media. Serial dilutions were performed (in neutralizing table (29); Bacillus cereus (FSL H3-272) was isolated from a buffer then phosphate-buffered saline [PBS] as described below) commercial milk plant filler spout. Optimal growth temperatures on initial aqueous inoculum to determine starting concentration. Њ were determined to be 30 C for P. fluorescens and B. cereus and Twelve pieces of film (1 by 1 cm2) were placed in a sterile Њ 37 C for E. coli and L. monocytogenes. Tryptic soy broth (TSB), culture tube, to which 1 ml of inoculum was added. The nature Bacto agar, and Difco neutralizing buffer were obtained from Bec- of the film surfaces in conjunction with the rotation of the tubes ton Dickinson (Sparks, Md.). Tryptic soy agar (TSA) was pre- ensured a distribution of liquid between the films and prevented pared by dissolving 30 g TSB, 15 g Bacto agar, and 20 g sodium stacking. After 15 min to 8 h rotating incubation at 30 or 37ЊC, chloride in 1 liter of ultrapure deionized water. All reagents used 50 ␮l of bacterial suspension was diluted in 450 ␮l of neutralizing Њ for microbiological testing were autoclaved at 121 C for 25 min. buffer, forming an initial 1:10 dilution, followed by serial dilutions Polyethylene surface modification. PE films were cleaned in PBS. One hundred microliters of each dilution was spread onto Њ and modified as previously described (19). Briefly, they were ox- TSA plates, which were then incubated at 30 or 37 C. After 24 idized by chromic acid to produce PE-COOH surface function- to 48 h, colonies were counted, and means were calculated from ality, then aminated with polyethylenimine to produce PE- three independent determinations. Unmodified PE films, unchlorinated PE-polyCOOH films, and inoculum without films served polyNH2 surface functionality, and finally further functionalized with polyacrylic acid to produce PE-polyCOOH surfaces. N-Hal- as controls. To evaluate rechargeability, films that had already amines were generated by shaking PE-polyCOOH films in 3,000 been tested for antimicrobial activity were vortexed three times in ppm of NaOCl aqueous solution for 15 min, followed by rinsing deionized water, followed by 1 min of vortexing in Foam Force in copious water. Figure 1 illustrates the proposed chlorination LP. Films were again vortexed three times in deionized water and mechanism of the PE-polyCOOH films. then placed in 3,000 ppm of NaOCl in deionized water for 15 min. Recharged films were shaken for 60 min at 37ЊCina106 to Charging and quantification of surface chlorine. Experi- 107 CFU/ml aqueous suspension of E. coli K-12, and antimicro- ments were conducted using chlorine demand–free glassware, bial activity was assessed via serial dilutions and plating as before. 2044 GODDARD AND HOTCHKISS J. Food Prot., Vol. 71, No. 10

of irreversible chlorination or chlorine-induced oxidation of secondary and tertiary amines present on PE-polyNH2 films (4, 17), with the plateau suggesting the formation of N-halamines on the amide bonds formed between polyethylenimine and PE-COOH surfaces, which are fewer in number than the amide bonds formed between polyacrylic acid and PE-polyNH2 surfaces. After4hofdrying over anhydrous calcium sulfate, PE-polyCOOH-Cl films retained 5.9 Ϯ 0.6 nmol/cm2 chlorine (n ϭ 4, ϮSD), which suggests storage stability without reduction in antimicrobial activity. To ob- serve the release of chlorine into pure water, PE-poly- COOH-Cl films (n ϭ 4) were shaken in reagent-grade de-

ionized water for 1, 2, 5, 10, 30, and 60 min. Less than Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/10/2042/2204454/0362-028x-71_10_2042.pdf by guest on 02 October 2021 0.15 nmol/cm2 chlorine migrated into water during any FIGURE 2. Rechargeability of control and modified polyethyl- time period, and after more than 100 min of shaking in ene films. Values are means of four independent films (n ϭ 4, deionized water, PE-polyCOOH-Cl films retained 5.3 Ϯ 0.3 ϮSE). nmol/cm2 chlorine, indicating that PE-polyCOOH-Cl will only release chlorine in the presence of microorganisms or other organic matter. To evaluate antimicrobial activity of the functionalized films in the presence of organic matter, a 104 to 105 CFU/ml inoculum of Antimicrobial activity. For all four tested organisms, E. coli K-12 was prepared in 10% TSB. Samples (1 ml) were significant (P Ͻ 0.05) reductions in microbial populations 2 shaken with and without 12 pieces of film (1 by 1 cm ), and serial were observed at each successive time point until the pop- dilutions were made at 0, 1, 2, 4, 8, and 12 h. ulations were too few to count. After 60 min, the microbial Statistical analyses. Chlorine rechargeability assays were load of aqueous suspensions of E. coli K-12, L. monocy- conducted in quadruplicate (four independent film samples, each togenes, and B. cereus in contact with PE-polyCOOH-Cl analyzed in a separate vial for chlorine retention). Antimicrobial films was reduced from ϳ106 CFU/ml to too few to count activity assays were conducted in triplicate (three independent (Ͻ102 CFU/ml), indicating a minimum 4-log reduction tubes, each containing 12 pieces of control or treated film [1 by (Fig. 3). PE-polyCOOH-Cl films also exhibited antimicro- 2 1cm]). Microbial populations were recorded and data were log bial activity against P. fluorescens, but at a slower rate, transformed for subsequent analyses. To determine antimicrobial requiring4htoreach too few to count. Pseudomonads are activity of chlorine-charged halamine film, one-way analysis of variance (ANOVA) followed by Tukey’s pairwise comparisons known for their metabolic diversity and their ability to was conducted on means of microbial populations incubated with thrive in a range of environmental conditions (16). Certain chlorine-charged halamine film (PE-polyCOOH-Cl). Unchlorinat- strains of Pseudomonas aeruginosa have been reported to ed halamine film (PE-polyCOOH), as well as unmodified PE film survive in chlorinated water (21). Because the tested P. (PE), served as controls. Film was considered to have exhibited fluorescens originated from a valve in a dairy plant, it is antimicrobial activity if the difference in means of microbial pop- likely that this particular isolate was less sensitive to chlo- ulations at successive time points was significant (P Ͻ 0.05). To rine. Neither the unmodified PE nor the unchlorinated PE- evaluate growth inhibition in dilute broth suspensions, means of polyCOOH control exhibited antimicrobial activity against microbial populations with and without chlorine-charged halamine E. coli K-12, P. fluorescens, or L. monocytogenes (P Ͼ functionalized film were compared at each time point with an 0.05), indicating that the observed antimicrobial activity unpaired t test. Growth inhibition was considered to have occurred if the difference between the populations was significant (P Ͻ was a result of N-halamine formation and that cell surface 0.05) at a particular time point. Statistical analyses were con- interactions were not a factor. The subtle growth inhibition ducted with GraphPad PRISM (GraphPad Software, San Diego, of B. cereus by PE films in the first hour of the study (P Calif.), which was also used to generate graphs. Ͻ 0.05) was likely a result of a hydrophobic interaction. Nevertheless, Tukey’s pairwise comparison indicates that RESULTS AND DISCUSSION the PE-polyCOOH-Cl films contributed significant (P Ͻ Chlorine rechargeability. PE-polyCOOH films were 0.05) antimicrobial activity against B. cereus after 1 h. able to recharge the N-halamine structures for all six rep- E. coli K-12 was chosen as the model organism for etitions, maintaining a total chlorine charge of 4.8 to 7.3 further antimicrobial activity assays. To better assess mi- nmol/cm2 (Fig. 2). PE and PE-COOH controls did not ex- crobial inactivation, PE-polyCOOH-Cl films were rotated hibit chlorine binding or release above detectable levels. in an aqueous suspension of 106 to 107 CFU/ml E. coli This indicates that the presence of chlorine on the PE- K-12, and dilutions were plated at 0, 15, 30, 60, and 90 polyCOOH and PE-polyNH2 films was not a result of car- min (Fig. 4). A greater than 2-log reduction was achieved ryover from the chlorine charging solution. The chlorine within 15 min rotation, and a greater than 5-log reduction rechargeability observed in PE-polyNH2 films followed an was achieved after 60 min. The antimicrobial activity of apparent exponential decay, presenting 3.5 nmol/cm2 total PE-polyCOOH-Cl films after successive uses, followed by chlorine initially and reaching a plateau of less than 1.5 washing in sanitizing solution and recharging in sodium nmol/cm2 after four charges. The decay might be a result hypochlorite solution, was also investigated (Fig. 5). After J. Food Prot., Vol. 71, No. 10 RECHARGEABLE ANTIMICROBIAL POLYETHYLENE 2045

FIGURE 3. Antimicrobial activity of control and modified films against E. coli K-12, P. fluorescens, L. monocytogenes, and B. cereus. Values are means of three determinations (n ϭ 3, ϮSE). Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/10/2042/2204454/0362-028x-71_10_2042.pdf by guest on 02 October 2021

an initial reduction of 5 to 6 log, PE-polyCOOH-Cl films hour of incubation, bacterial suspensions incubated with the maintained sufficient antimicrobial activity to achieve at PE-polyCOOH-Cl films maintained 0.5- to 1.5-log fewer least a reduction of 3 to 4 log for four successive uses, organisms (CFU per milliliter) than the control over the suggesting that the modified polyethylene films are capable 12-h test period. As determined by t test at each time point, of providing rechargeable antimicrobial activity. The ob- microbial populations incubated with the treated films were served decrease in activity could be a result of Hoffman significantly lower (P Ͻ 0.05) than those incubated without degradation of the amide linkages, which occurs in certain the films throughout the course of the study. This result alkaline solutions, such as those used in some sanitizing suggests that in the presence of dilute organic matter, the agents (4). PE-polyCOOH-Cl films reduced microbial growth. How- To evaluate the antimicrobial effectiveness of PE- ever, chlorine is known to be less effective in the presence polyCOOH-Cl films in the presence of organic matter, sus- of organic matter. pensions of 104 to 105 CFU/ml of E. coli K-12 in 10% As described in the introduction, there are two potential TSB were rotated with and without PE-polyCOOH-Cl mechanisms by which N-halamine structures could exhibit films, and dilutions were plated at 0, 1, 2, 4, 8, and 12 h (Fig. 6). After an initial 0.25-log reduction within the first

FIGURE 5. Rechargeability of PE-polyCOOH-Cl: antimicrobial FIGURE 4. Antimicrobial activity of PE-polyCOOH-Cl against activity of PE-polyCOOH-Cl against E. coli K-12 after successive E. coli K-12. Values are means of three determinations (n ϭ 3, uses, washes, and rechlorination. Values are means of three de- ϮSE). terminations (n ϭ 3, ϮSE). 2046 GODDARD AND HOTCHKISS J. Food Prot., Vol. 71, No. 10

ment 2002-38420-11738. The authors gratefully acknowledge Dr. Kathryn J. Boor and Dr. Martin Wiedmann of the Cornell University Food Science Food Safety Laboratory for providing isolates, materials, and technical assistance.

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