Preliminary Efficacy Testing of the Disinfectant MicrobeCare XLP for Potential Use in Military Operational Environments

Preliminary Efficacy Testing of the Disinfectant MicrobeCare XLP for Potential Use in Military... Abstract Introduction A safe, easy-to-use, permanently bonded antiseptic that does not require post-exposure bioload reduction but maintains effectiveness over time would have far-reaching implications across multiple industries. Health care is one such arena, particularly in austere military settings where resources are at a premium. MicrobeCare XLP (MicrobeCare, Buffalo Grove, IL, USA) is a commercially available spray-on agent that is advertised to covalently bond to surfaces and provide a long-lasting antimicrobial coating inhospitable to >99.99% of surface microorganisms. A pilot study was devised to gather baseline data regarding product efficacy and laboratory parameters before consideration of extended investigations and military utilization. The product manufacturer recommends bioload reductions before product application, following product application, and after each pathogenic exposure. To investigate the product’s efficacy in circumstances more closely simulating a military operational setting in which post-pathogenic exposure bioload reduction would not be possible, this step was deliberately excluded from the test sequences. Materials and Methods Using autoclaved surgical forceps, growth of Staphylococcus aureus and Acinetobacter baumannii was evaluated in a controlled manner under multiple conditions. Test variations included duration of submersion in the MicrobeCare XLP solution and air-drying and a second autoclave sterilization. Control and treated forceps were exposed to a bacterial suspension and air-dried before being submerged in sterile saline and vortex mixed. The saline solution was serially diluted and plated on tryptic soy agar (TSA) II plates. Plates were incubated for 24 h and bacterial colony-forming units (CFU)/mL were counted. Results Statistical significance was defined according to the American Society for Testing and Materials (ASTM) International passing criteria of 3 Log10 or 99.9% reduction of microorganisms. Additionally, p-values were calculated using two-tailed unpaired two-sample t-tests with unequal variance with a threshold of 0.05. In the S. aureus tests, none of the reduction calculations met the ASTM International passing criteria. In addition, the difference between the means of the colony counts in the MicrobeCare XLP-treated forceps and untreated control forceps was not statistically significant (p-value 0.109). Conversely, in the A. baumannii tests, each of the percent reduction calculations met the ASTM International passing criteria; the difference between the means of the colony counts in the treatment and control groups was statistically significant (p-value 0.008). Conclusion In these independent tests, MicrobeCare XLP effectively prevented growth of A. baumannii but had unpredictable results suppressing S. aureus. These results may relate to inherent properties of the bacteria or autoclave exposure, although the manufacturer asserts that the coating withstands such degradation. Additional testing could be performed using a broader range of microorganisms and exposure to varying conditions including other sterilization methods. INTRODUCTION Significance and Military Relevance MicrobeCare XLP is a commercially available spray-on product that reportedly incorporates quaternary ammonium cations to affect comprehensive bactericidal activity, in addition to directly killing viruses, fungi, and algae. It is marketed as a permanent antimicrobial barrier that can be easily applied to nearly any surface. If this product were to perform as advertised, it would have a myriad of potential applications. Such a tool would be particularly valuable in the operational military environment where pre-treated equipment could improve infection control in settings where traditional sterilization techniques are impractical or impossible. Conceivably, a permanent antimicrobial treatment could reduce or eliminate the need to carry large quantities of antiseptics and water for disinfection aboard MEDEVAC aircraft, freeing up carrying capacity for additional medical supplies or even additional patients. Furthermore, application of such a product to high-traffic or frequently touched areas such as patient litters, operating tables, and surgical instruments could pose an effective means to reduce rates of iatrogenic infection. Given the possibilities raised by the MicrobeCare XLP manufacturers’ claims, we independently evaluated its efficacy specifically without performing post-pathogenic exposure bioload reduction to more closely simulate practical usage in theater. Background and Review of Literature The active ingredient in MicrobeCare XLP is a quaternary ammonium compound (QAC). Various forms of QACs have been used as disinfectants in the food service and health care industries since their introduction in the late 1930s; MicrobeCare claims to incorporate a new and more effective version of this well-established technology. Chemically, QACs are organically substituted ammonium compounds with known bactericidal, virucidal, and fungicidal activity.1 The bactericidal action of these compounds has been attributed to several incompletely characterized mechanisms including denaturation of essential cell proteins and disruption of the cell membrane.2,3 Recent studies have demonstrated that QACs in solution may directly kill microorganisms through a different mechanism than QACs immobilized on a surface. Although QACs in solution are thought to interdigitate over the entire surface of a bacterium, it has been proposed that immobilized QACs cause cell death by inducing lethally strong attractive forces between bacteria and the QAC-coated surface.4 MicrobeCare XLP is a QAC coating that purportedly creates covalent bonds to surfaces where it is applied. A study published by the manufacturer demonstrated that the product retained antimicrobial activity following accelerated age testing equivalent to 12 yr of cleaning at a hospital.5 Despite the long history of QAC use in antimicrobial applications, previous studies have demonstrated variable results regarding their antimicrobial activity. Attempts to reproduce results reported by product manufacturers have been inconsistent and much of the existing literature addressing the efficacy of QACs as disinfectants is dated.6,7,8 Many of these studies were conducted decades ago and may not be applicable to the more recently developed fourth- and fifth-generation QACs. Furthermore, recent studies have demonstrated the development of bacterial resistance against QACs,9 which is an important consideration if MicrobeCare XLP is to be considered for military use. In light of shortcomings in the existing literature and the exciting possibilities raised by the MicrobeCare XLP manufacturer’s claims, we set out to independently evaluate its efficacy against representative Gram-positive and Gram-negative bacteria of medical significance. MATERIALS AND METHODS To investigate the antibacterial efficacy of MicrobeCare XLP, we conducted a pilot study comparing growth of Staphylococcus aureus and Acinetobacter baumannii on surgical forceps using several predetermined cleansing and sterilization sequences. There were several steps that were replicated in each sequence. The initial sterilization procedure remained constant: two identical surgical forceps were sterilized in separate pouches using a Getinge Model 533LS autoclave system (Getinge AB, Gothenburg, Sweden). Sterilization was conducted using wet heat at a pressure of 15 PSI, an internal temperature at peak autoclave of 121°C, and a holding time of 30 min. When the treatment group forceps were submerged in MicrobeCare XLP, a standard 12-mL volume was used. Intermediate steps varied in the duration of submersion in the MicrobeCare XLP solution and air-drying, and whether a second autoclave sterilization was included. These intermediate steps are individually described in more detail below in association with their respective test sequence (S1–9 or A1–6). The final preparation steps were constant. Separately, the treatment and control forceps were each submerged in 12 mL of 1.5 × 106 CFU/mL of bacteria (either S. aureus 25923 or A. baumannii BAA 747) for 30 min and allowed to air-dry for 30 min. After bacterial exposure, each pair of forceps was submerged in 10 mL of 0.9% sterile saline, vortex mixed for 2 min, and removed from the saline. The saline was then serially diluted 1:10 and plated on TSA II 5% sheep blood agar; plates were incubated at 35°C for 24 h in an aerobic environment. Colony counts were then performed. As mentioned previously, the intermediate steps are performed when test alterations occurred. Variations included initial duration of submersion in the MicrobeCare XLP solution (5 or 2 min), length of time spent air-drying (24 h or 2 min), duration of repeat submersion in the MicrobeCare XLP solution (5 or 2 min), time spent air-drying again (5 or 2 min), and whether forceps were autoclaved a second time. The second autoclave exposure was meant to represent bioload reduction as suggested by the manufacturers before equipment use. This was purposefully excluded from most of the test sequences to replicate practical use in a military environment; however, it was included in tests S1–2 and A6. A flowchart illustrating the variations in testing protocols for both the S. aureus and the A. baumannii groups is provided below (Fig. 1). Figure 1. View largeDownload slide Bacterial testing protocol. Figure 1. View largeDownload slide Bacterial testing protocol. For the first S. aureus test (labeled Test S1 in results below), the treatment group forceps were prepared by submersion in MicrobeCare XLP for 5 min followed by a 24-h period of air-drying. Then, the treated forceps were re-submerged in 12 mL of MicrobeCare XLP for 5 min, air-dried for 5 min, and buffed with sterile gauze. The treated forceps were sterilized a second time under the same autoclave conditions after the repeat coating with MicrobeCare XLP before the standard bacterial exposure and isolation steps. This same sequence was duplicated in Test S2. In Tests S3 and S4, the treated forceps were submerged in MicrobeCare XLP for 5 min, air-dried for 24 h, re-submerged in MicrobeCare XLP for 5 min, air-dried for 5 min, and then buffed with sterile gauze before being exposed to S. aureus. In Tests S5, S6, and S7, the treated forceps were submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, re-submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, and then buffed with sterile gauze before bacterial exposure. In Tests S8 and S9, the treated forceps were submerged in MicrobeCare XLP for 5 min, air-dried for 24 h, re-submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, buffed with sterile gauze, and then exposed to S. aureus. For Tests S3 through S9, the treated pairs of forceps were not autoclaved a second time after the initial treatment with MicrobeCare XLP. Following initial autoclave sterilization, A. baumannii growth was tested in a similar manner to that described for S. aureus. In Tests A1 and A2, each forcep was submerged in MicrobeCare XLP for 5 min, air-dried for 24 h, re-submerged in MicrobeCare XLP for 5 min, air-dried for 2 min, buffed with sterile gauze, and then exposed to A. baumannii with subsequent colony counts performed as described above. In Tests A3, A4, and A5, the forceps were submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, re-submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, and then buffed with sterile gauze before A. baumannii exposure. In Test A6, the forceps were submerged in MicrobeCare XLP for 2 min, air-dried for 24 h, re-submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, and buffed with sterile gauze. The A6 test group was the only one to undergo a second autoclave sterilization before A. baumannii exposure. RESULTS In the S. aureus groups, a higher bacterial yield was observed in the untreated controls compared with the MicrobeCare XLP-treated instruments in seven of the nine tests (77.8%, refer to Fig. 1). However, none of the reduction calculations met the American Society for Testing and Materials (ASTM) International passing criteria of 3 Log10 or 99.9%. In two of the nine tests (S1 and S5), increased bacterial growth occurred on the MicrobeCare XLP-treated forceps in comparison with the control forceps. Tests S3 and S4 included the shortest intervals for MicrobeCare XLP submersion and drying times (2 min each for two cycles) and did not undergo a second autoclave sterilization. Reduction calculations for these tests were the highest in the S. aureus groups, although they did not meet the specified requirements (S3 = 99.3% and S4 = 99.6%). Overall, the S. aureus untreated control forceps data set demonstrated particularly low concordance as depicted by Figure 2, with multiple extreme outlier values resulting in a mean (2.41 × 104) outside of the interquartile range. The mean colony count for the S. aureus MicrobeCare XLP-treated group was 8.56 × 103, compared with 2.41 × 104 for the control group; however, the difference was not statistically significant (p-value 0.109 by two-tailed unpaired two-sample t-test with unequal variance). Figure 2. View largeDownload slide S. aureus and A. baumannii colony counts on MicrobeCare XLP-treated and untreated control forceps. Figure 2. View largeDownload slide S. aureus and A. baumannii colony counts on MicrobeCare XLP-treated and untreated control forceps. In contrast, no growth of A. baumannii was observed on the MicrobeCare XLP-treated forceps in any of the tests performed. The overall minimum value in colony counts for the A. baumannii untreated control forcep group belonged to A6, which was the only series in the A. baumannii tests where the forceps underwent two autoclave treatments. The mean of the colony counts from the untreated control forceps was 7.28 × 103 across the six test series. All of the percent reduction calculations met the ASTM International passing criteria; the Log10 values could not be calculated. In addition, the difference between the means of the colony counts in the A. baumannii MicrobeCare XLP-treated forceps and untreated control forcep groups was statistically significant (p-value 0.008 by two-tailed unpaired two-sample t-test with unequal variance). Table I. S. aureus and A. baumannii Colony Counts on MicrobeCare XLP-treated and Untreated Control Forceps S. aureus  A. baumannii  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Treated forceps  Untreated control forceps  Percent (%)  Log10  Treated forceps  Untreated control forceps  Percent (%)  Log10  S1  2.51 × 104 (max)  3.70 × 103  −578.4  −0.8  A1  0  5.10 × 103  100.0  NA  S2  7.80 × 103  1.00 × 104  22.0  0.1  A2  0  1.44 × 104 (max)  100.0  NA  S3  1.20 × 102  1.66 × 104  99.3  2.1  A3  0  5.50 × 103  100.0  NA  S4  9.00 × 101 (min)  2.32 × 104  99.6  2.4  A4  0  9.70 × 103  100.0  NA  S5  9.20 × 103  1.80 × 103 (min)  −411.1  −0.7  A5  0  6.30 × 103  100.0  NA  S6  1.90 × 102  1.63 × 104  98.8  1.9  A6  0  2.70 × 103 (min)  100.0  NA  S7  9.00 × 103  4.90 × 104 (OL)  81.6  0.7            S8  8.50 × 103  1.65 × 104  48.5  0.3            S9  1.70 × 104  8.00 × 104 (max)  78.8  0.7            Median  8.50 × 103  1.65 × 104      Median  0  5.90 × 103      Mean  8.56 × 103  2.41 × 104      Mean  0  7.28 × 103      S. aureus  A. baumannii  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Treated forceps  Untreated control forceps  Percent (%)  Log10  Treated forceps  Untreated control forceps  Percent (%)  Log10  S1  2.51 × 104 (max)  3.70 × 103  −578.4  −0.8  A1  0  5.10 × 103  100.0  NA  S2  7.80 × 103  1.00 × 104  22.0  0.1  A2  0  1.44 × 104 (max)  100.0  NA  S3  1.20 × 102  1.66 × 104  99.3  2.1  A3  0  5.50 × 103  100.0  NA  S4  9.00 × 101 (min)  2.32 × 104  99.6  2.4  A4  0  9.70 × 103  100.0  NA  S5  9.20 × 103  1.80 × 103 (min)  −411.1  −0.7  A5  0  6.30 × 103  100.0  NA  S6  1.90 × 102  1.63 × 104  98.8  1.9  A6  0  2.70 × 103 (min)  100.0  NA  S7  9.00 × 103  4.90 × 104 (OL)  81.6  0.7            S8  8.50 × 103  1.65 × 104  48.5  0.3            S9  1.70 × 104  8.00 × 104 (max)  78.8  0.7            Median  8.50 × 103  1.65 × 104      Median  0  5.90 × 103      Mean  8.56 × 103  2.41 × 104      Mean  0  7.28 × 103      Table I. S. aureus and A. baumannii Colony Counts on MicrobeCare XLP-treated and Untreated Control Forceps S. aureus  A. baumannii  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Treated forceps  Untreated control forceps  Percent (%)  Log10  Treated forceps  Untreated control forceps  Percent (%)  Log10  S1  2.51 × 104 (max)  3.70 × 103  −578.4  −0.8  A1  0  5.10 × 103  100.0  NA  S2  7.80 × 103  1.00 × 104  22.0  0.1  A2  0  1.44 × 104 (max)  100.0  NA  S3  1.20 × 102  1.66 × 104  99.3  2.1  A3  0  5.50 × 103  100.0  NA  S4  9.00 × 101 (min)  2.32 × 104  99.6  2.4  A4  0  9.70 × 103  100.0  NA  S5  9.20 × 103  1.80 × 103 (min)  −411.1  −0.7  A5  0  6.30 × 103  100.0  NA  S6  1.90 × 102  1.63 × 104  98.8  1.9  A6  0  2.70 × 103 (min)  100.0  NA  S7  9.00 × 103  4.90 × 104 (OL)  81.6  0.7            S8  8.50 × 103  1.65 × 104  48.5  0.3            S9  1.70 × 104  8.00 × 104 (max)  78.8  0.7            Median  8.50 × 103  1.65 × 104      Median  0  5.90 × 103      Mean  8.56 × 103  2.41 × 104      Mean  0  7.28 × 103      S. aureus  A. baumannii  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Treated forceps  Untreated control forceps  Percent (%)  Log10  Treated forceps  Untreated control forceps  Percent (%)  Log10  S1  2.51 × 104 (max)  3.70 × 103  −578.4  −0.8  A1  0  5.10 × 103  100.0  NA  S2  7.80 × 103  1.00 × 104  22.0  0.1  A2  0  1.44 × 104 (max)  100.0  NA  S3  1.20 × 102  1.66 × 104  99.3  2.1  A3  0  5.50 × 103  100.0  NA  S4  9.00 × 101 (min)  2.32 × 104  99.6  2.4  A4  0  9.70 × 103  100.0  NA  S5  9.20 × 103  1.80 × 103 (min)  −411.1  −0.7  A5  0  6.30 × 103  100.0  NA  S6  1.90 × 102  1.63 × 104  98.8  1.9  A6  0  2.70 × 103 (min)  100.0  NA  S7  9.00 × 103  4.90 × 104 (OL)  81.6  0.7            S8  8.50 × 103  1.65 × 104  48.5  0.3            S9  1.70 × 104  8.00 × 104 (max)  78.8  0.7            Median  8.50 × 103  1.65 × 104      Median  0  5.90 × 103      Mean  8.56 × 103  2.41 × 104      Mean  0  7.28 × 103      DISCUSSION Antibacterial Efficacy Differing patterns of growth of S. aureus and A. baumannii were observed following treatment with MicrobeCare XLP in the testing sequences. S. aureus growth was particularly unpredictable: even test pairs that followed identical procedures (i.e., S8 and S9) demonstrated strikingly different results. Notably, growth of at least some S. aureus was detected on the MicrobeCare XLP-treated forceps in every test. Although some of the test series approached the ASTM guidelines for significance (in particular S3 and S4), none met or exceeded the requirements. The A. baumannii tests, in contrast, demonstrated no bacterial growth on the MicrobeCare XLP-treated forceps in any of the six tests performed. It is conceivable that differences in the cell wall structure between the gram-positive S. aureus and the gram-negative A. baumannii could account for these observed differences in MicrobeCare XLP’s efficacy. As discussed above, however, the mechanism of action of quaternary ammonium compounds remains unclear. Testing of other bacterial species would be necessary to draw a broader conclusion about whether or not MicrobeCare XLP is truly more effective at preventing gram-negative than gram-positive bacterial colonization. Logical bacteria to include in further testing could include Enterococcus faecium, Pseudomonas aeruginosa, and Enterobacter spp., which together (along with A. baumannii and S. aureus) compose the ESKAPE pathogens, a group of virulent bacteria that are responsible for the majority of nosocomial infections worldwide and commonly exhibit multi-drug antibiotic resistance.10,11 Influence of Repeat Autoclave Exposure In Tests S1 and S2 of the S. aureus experiments, the surgical forceps were subjected to a second sterilization via autoclave following the application of MicrobeCare XLP, which represented post-treatment bioload reduction. Surprisingly, Test S1 demonstrated a maximum value in colony counts among the MicrobeCare XLP-treated forceps exposed to S. aureus (2.51 × 104). Six of the other seven tests in which the forceps were only autoclaved before the MicrobeCare XLP application demonstrated higher bacterial counts from the untreated controls compared with the treated forceps. Tests S3 and S4 did not undergo a second autoclave sterilization and reduction calculations for these tests were the highest in the S. aureus groups (S3 = 99.3% and S4 = 99.6%). Although the reductions in microorganisms counts never reached the ASTM threshold for significance, these results suggested that MicrobeCare XLP was more effective against S. aureus after only a single autoclave sterilization. However, a similar decrease in efficacy was not observed in the A. baumannii test in which the forceps received two autoclave treatments (Test A6). This test also produced the overall minimum value in colony counts for the A. baumannii untreated control forceps group. We are therefore unable to definitively conclude that the additional autoclave exposure was the cause of the increased bacterial growth observed in the treatment group of S. aureus Tests S1, and the insignificant reduction of microorganisms in S2, based on these results alone. Additionally, the manufacturer offers data supporting the assertion that a MicrobeCare XLP coating can withstand a wide range of hospital-setting-cleansing practices such as routine terminal cleanings with a quaternary disinfectant,12 in addition to a variety of commonly used commercial disinfectant wipes and solutions including full-strength bleach.5 Given the inconsistencies between the manufacturer’s reports, the results obtained in our study, and historical data showing that QACs degrade over time,13 further testing is warranted to determine the efficacy of this product throughout different cleansing and sterilization procedures. Specifically, the addition of another commercially available disinfectant in a positive control group may be considered. Potential Impact of Post-exposure Bioload Reduction Although our group tested the MicrobeCare XLP product in a manner similar to other tests referenced in the product’s executive summary, we did not perform a bioload reduction step following pathogenic exposure as recommended. Our methodology specifically withheld this step as we were interested in the product’s use in resource-limited settings where post-exposure bioload reduction may be impractical or impossible. It is possible that the lack of bioload reduction following bacterial exposure limited the effectiveness of the product. This tertiary bioload reduction step may be incorporated into additional protocols to make a conclusion about its necessity and to represent typical clinical use. CONCLUSION During our evaluation of MicrobeCare XLP, we observed that the product was effective in preventing colonization by A. baumannii in several predetermined laboratory scenarios; the reduction in microorganisms between the treated and untreated control groups met both the ASTM International passing criteria and the traditional threshold of statistical significance. MicrobeCare XLP treatment did not lead to a statistically significant reduction of S. aureus by either calculation. Further testing of this product is warranted to fully evaluate its practical utility in a military operational environment. Additional studies could include a control group that undergoes post-exposure microbial load reduction, another disinfectant as a positive control, a wider range of health-care-associated pathogenic organisms, as well as other cleansing and sterilization processes. Funding Funding for this project was provided by the United States Air Force Clinical Investigator Program at the 59 Medical Wing at JBSA-Lackland, TX, and all laboratory evaluation was conducted at the 59th Clinical Research Division Laboratory at the 59th Medical Wing, JBSA-Lackland, TX. References 1 Rutala WA, Weber DJ, the Healthcare Infection Control Practices Advisory Committee (HICPAC). Guideline for disinfection and sterilization in healthcare facilities ( 2008). Centers for Disease Control and Prevention. https://www.cdc.gov/infectioncontrol/guidelines/Disinfection/index.html. Accessed October 26, 2017. 2 Merianos JJ: Surface-active agents. In: Disinfection, Sterilization, and Preservation , pp 283– 320. Edited by Block SS Philadelphia, PA, Lippincott Williams & Wilkins, 2001. 3 Petrocci AN: Surface active agents: quaternary ammonium compounds. In: Disinfection, Sterilization, and Preservation , pp 309– 29. Edited by Block SS, Philadelphia, PA, Lea & Febiger, 1983. 4 Asri LATW, Crismaru M, Roest S, Chen Y, Ivashenko O, Rudolf P, Tiller JC, van der Mei HC, Loontjens TJ A, Busscher HJ: A shape-adaptive, antibacterial-coating of immobilized quaternary-ammonium compounds tethered on hyperbranched polyurea and its mechanism of action. Adv Funct Mater  2014; 24: 346– 55. Google Scholar CrossRef Search ADS   5 Accelerated age testing with MicrobeCare with Ohio medical push to set suction regulators. MicrobeCareTM website. http://www.microbecare.com/wp-content/uploads/2015/10/Accelerated-Age-Testing-with-MicrobeCare.pdf. Accessed October 24, 2017. 6 Rutala WA, Cole EC: Ineffectiveness of hospital disinfectants against bacteria: a collaborative study. Infect Control  1987; 8: 501– 6. Google Scholar CrossRef Search ADS PubMed  7 Cole EC, Rutala WA, Samsa GP.: Disinfectant testing using a modified use-dilution method: collaborative study. J Assoc Off Anal Chem  1988; 71: 1187– 94. Google Scholar PubMed  8 Rutala WA, Cole EC, Wannamaker NS, Weber DJ: Inactivation of Mycobacterium tuberculosis and Mycobacterium bovis by 14 hospital disinfectants. Am J Med  1991; 91: 267S– 71S. Google Scholar CrossRef Search ADS PubMed  9 Jennings MC, Buttaro BA, Minbiole KPC, Wuest WM: Bioorganic investigation of multicationic antimicrobials to combat QAC-resistant Staphylococcus aureus. ACS Infect Dis  2015; 1( 7): 304– 9. Google Scholar CrossRef Search ADS PubMed  10 Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J: Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis  2009; 48( 1): 1– 12. Google Scholar CrossRef Search ADS PubMed  11 Santajit S, Indrawattana N: Mechanisms of antimicrobial resistance in ESKAPE pathogens. BioMed Res Int  2016; 2016: 2475067. Google Scholar CrossRef Search ADS PubMed  12 Lewis BD, Spencer M, Rossi PJ, Lee CJ, Brown KR, Malinowski M, Seabrook GR, Edmiston CE Jr: Assessment of an innovative antimicrobial surface disinfectant in the operating room environment using adenosine triphosphate bioluminescence assay. Am J Infect Control  2015; 43( 3): 283– 5. MicrobeCareTM website. http://www.microbecare.com/wp-content/uploads/2016/07/Lewis-et-al-2015-Am-J-Infection-Control.pdf. Accessed October 24, 2017. Google Scholar CrossRef Search ADS PubMed  13 Tezel U, Pavlostathis SG: Quaternary ammonium disinfectants: microbial adaptation, degradation and ecology. Curr Opin Biotechnol  2015; 33: 296– 304. Google Scholar CrossRef Search ADS PubMed  Author notes Opinions expressed are those of the authors and are not to be construed as official or as representing those of the U.S. Army, U.S. Air Force, the Department of Defense, or the U.S. Government. Mention of trade names, commercial products, or organizations does not imply endorsement by the U.S. Government. Published by Oxford University Press on behalf of the Association of Military Surgeons of the United States 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Military Medicine Oxford University Press

Preliminary Efficacy Testing of the Disinfectant MicrobeCare XLP for Potential Use in Military Operational Environments

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Association of Military Surgeons of the United States
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Published by Oxford University Press on behalf of the Association of Military Surgeons of the United States 2018.
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Abstract

Abstract Introduction A safe, easy-to-use, permanently bonded antiseptic that does not require post-exposure bioload reduction but maintains effectiveness over time would have far-reaching implications across multiple industries. Health care is one such arena, particularly in austere military settings where resources are at a premium. MicrobeCare XLP (MicrobeCare, Buffalo Grove, IL, USA) is a commercially available spray-on agent that is advertised to covalently bond to surfaces and provide a long-lasting antimicrobial coating inhospitable to >99.99% of surface microorganisms. A pilot study was devised to gather baseline data regarding product efficacy and laboratory parameters before consideration of extended investigations and military utilization. The product manufacturer recommends bioload reductions before product application, following product application, and after each pathogenic exposure. To investigate the product’s efficacy in circumstances more closely simulating a military operational setting in which post-pathogenic exposure bioload reduction would not be possible, this step was deliberately excluded from the test sequences. Materials and Methods Using autoclaved surgical forceps, growth of Staphylococcus aureus and Acinetobacter baumannii was evaluated in a controlled manner under multiple conditions. Test variations included duration of submersion in the MicrobeCare XLP solution and air-drying and a second autoclave sterilization. Control and treated forceps were exposed to a bacterial suspension and air-dried before being submerged in sterile saline and vortex mixed. The saline solution was serially diluted and plated on tryptic soy agar (TSA) II plates. Plates were incubated for 24 h and bacterial colony-forming units (CFU)/mL were counted. Results Statistical significance was defined according to the American Society for Testing and Materials (ASTM) International passing criteria of 3 Log10 or 99.9% reduction of microorganisms. Additionally, p-values were calculated using two-tailed unpaired two-sample t-tests with unequal variance with a threshold of 0.05. In the S. aureus tests, none of the reduction calculations met the ASTM International passing criteria. In addition, the difference between the means of the colony counts in the MicrobeCare XLP-treated forceps and untreated control forceps was not statistically significant (p-value 0.109). Conversely, in the A. baumannii tests, each of the percent reduction calculations met the ASTM International passing criteria; the difference between the means of the colony counts in the treatment and control groups was statistically significant (p-value 0.008). Conclusion In these independent tests, MicrobeCare XLP effectively prevented growth of A. baumannii but had unpredictable results suppressing S. aureus. These results may relate to inherent properties of the bacteria or autoclave exposure, although the manufacturer asserts that the coating withstands such degradation. Additional testing could be performed using a broader range of microorganisms and exposure to varying conditions including other sterilization methods. INTRODUCTION Significance and Military Relevance MicrobeCare XLP is a commercially available spray-on product that reportedly incorporates quaternary ammonium cations to affect comprehensive bactericidal activity, in addition to directly killing viruses, fungi, and algae. It is marketed as a permanent antimicrobial barrier that can be easily applied to nearly any surface. If this product were to perform as advertised, it would have a myriad of potential applications. Such a tool would be particularly valuable in the operational military environment where pre-treated equipment could improve infection control in settings where traditional sterilization techniques are impractical or impossible. Conceivably, a permanent antimicrobial treatment could reduce or eliminate the need to carry large quantities of antiseptics and water for disinfection aboard MEDEVAC aircraft, freeing up carrying capacity for additional medical supplies or even additional patients. Furthermore, application of such a product to high-traffic or frequently touched areas such as patient litters, operating tables, and surgical instruments could pose an effective means to reduce rates of iatrogenic infection. Given the possibilities raised by the MicrobeCare XLP manufacturers’ claims, we independently evaluated its efficacy specifically without performing post-pathogenic exposure bioload reduction to more closely simulate practical usage in theater. Background and Review of Literature The active ingredient in MicrobeCare XLP is a quaternary ammonium compound (QAC). Various forms of QACs have been used as disinfectants in the food service and health care industries since their introduction in the late 1930s; MicrobeCare claims to incorporate a new and more effective version of this well-established technology. Chemically, QACs are organically substituted ammonium compounds with known bactericidal, virucidal, and fungicidal activity.1 The bactericidal action of these compounds has been attributed to several incompletely characterized mechanisms including denaturation of essential cell proteins and disruption of the cell membrane.2,3 Recent studies have demonstrated that QACs in solution may directly kill microorganisms through a different mechanism than QACs immobilized on a surface. Although QACs in solution are thought to interdigitate over the entire surface of a bacterium, it has been proposed that immobilized QACs cause cell death by inducing lethally strong attractive forces between bacteria and the QAC-coated surface.4 MicrobeCare XLP is a QAC coating that purportedly creates covalent bonds to surfaces where it is applied. A study published by the manufacturer demonstrated that the product retained antimicrobial activity following accelerated age testing equivalent to 12 yr of cleaning at a hospital.5 Despite the long history of QAC use in antimicrobial applications, previous studies have demonstrated variable results regarding their antimicrobial activity. Attempts to reproduce results reported by product manufacturers have been inconsistent and much of the existing literature addressing the efficacy of QACs as disinfectants is dated.6,7,8 Many of these studies were conducted decades ago and may not be applicable to the more recently developed fourth- and fifth-generation QACs. Furthermore, recent studies have demonstrated the development of bacterial resistance against QACs,9 which is an important consideration if MicrobeCare XLP is to be considered for military use. In light of shortcomings in the existing literature and the exciting possibilities raised by the MicrobeCare XLP manufacturer’s claims, we set out to independently evaluate its efficacy against representative Gram-positive and Gram-negative bacteria of medical significance. MATERIALS AND METHODS To investigate the antibacterial efficacy of MicrobeCare XLP, we conducted a pilot study comparing growth of Staphylococcus aureus and Acinetobacter baumannii on surgical forceps using several predetermined cleansing and sterilization sequences. There were several steps that were replicated in each sequence. The initial sterilization procedure remained constant: two identical surgical forceps were sterilized in separate pouches using a Getinge Model 533LS autoclave system (Getinge AB, Gothenburg, Sweden). Sterilization was conducted using wet heat at a pressure of 15 PSI, an internal temperature at peak autoclave of 121°C, and a holding time of 30 min. When the treatment group forceps were submerged in MicrobeCare XLP, a standard 12-mL volume was used. Intermediate steps varied in the duration of submersion in the MicrobeCare XLP solution and air-drying, and whether a second autoclave sterilization was included. These intermediate steps are individually described in more detail below in association with their respective test sequence (S1–9 or A1–6). The final preparation steps were constant. Separately, the treatment and control forceps were each submerged in 12 mL of 1.5 × 106 CFU/mL of bacteria (either S. aureus 25923 or A. baumannii BAA 747) for 30 min and allowed to air-dry for 30 min. After bacterial exposure, each pair of forceps was submerged in 10 mL of 0.9% sterile saline, vortex mixed for 2 min, and removed from the saline. The saline was then serially diluted 1:10 and plated on TSA II 5% sheep blood agar; plates were incubated at 35°C for 24 h in an aerobic environment. Colony counts were then performed. As mentioned previously, the intermediate steps are performed when test alterations occurred. Variations included initial duration of submersion in the MicrobeCare XLP solution (5 or 2 min), length of time spent air-drying (24 h or 2 min), duration of repeat submersion in the MicrobeCare XLP solution (5 or 2 min), time spent air-drying again (5 or 2 min), and whether forceps were autoclaved a second time. The second autoclave exposure was meant to represent bioload reduction as suggested by the manufacturers before equipment use. This was purposefully excluded from most of the test sequences to replicate practical use in a military environment; however, it was included in tests S1–2 and A6. A flowchart illustrating the variations in testing protocols for both the S. aureus and the A. baumannii groups is provided below (Fig. 1). Figure 1. View largeDownload slide Bacterial testing protocol. Figure 1. View largeDownload slide Bacterial testing protocol. For the first S. aureus test (labeled Test S1 in results below), the treatment group forceps were prepared by submersion in MicrobeCare XLP for 5 min followed by a 24-h period of air-drying. Then, the treated forceps were re-submerged in 12 mL of MicrobeCare XLP for 5 min, air-dried for 5 min, and buffed with sterile gauze. The treated forceps were sterilized a second time under the same autoclave conditions after the repeat coating with MicrobeCare XLP before the standard bacterial exposure and isolation steps. This same sequence was duplicated in Test S2. In Tests S3 and S4, the treated forceps were submerged in MicrobeCare XLP for 5 min, air-dried for 24 h, re-submerged in MicrobeCare XLP for 5 min, air-dried for 5 min, and then buffed with sterile gauze before being exposed to S. aureus. In Tests S5, S6, and S7, the treated forceps were submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, re-submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, and then buffed with sterile gauze before bacterial exposure. In Tests S8 and S9, the treated forceps were submerged in MicrobeCare XLP for 5 min, air-dried for 24 h, re-submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, buffed with sterile gauze, and then exposed to S. aureus. For Tests S3 through S9, the treated pairs of forceps were not autoclaved a second time after the initial treatment with MicrobeCare XLP. Following initial autoclave sterilization, A. baumannii growth was tested in a similar manner to that described for S. aureus. In Tests A1 and A2, each forcep was submerged in MicrobeCare XLP for 5 min, air-dried for 24 h, re-submerged in MicrobeCare XLP for 5 min, air-dried for 2 min, buffed with sterile gauze, and then exposed to A. baumannii with subsequent colony counts performed as described above. In Tests A3, A4, and A5, the forceps were submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, re-submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, and then buffed with sterile gauze before A. baumannii exposure. In Test A6, the forceps were submerged in MicrobeCare XLP for 2 min, air-dried for 24 h, re-submerged in MicrobeCare XLP for 2 min, air-dried for 2 min, and buffed with sterile gauze. The A6 test group was the only one to undergo a second autoclave sterilization before A. baumannii exposure. RESULTS In the S. aureus groups, a higher bacterial yield was observed in the untreated controls compared with the MicrobeCare XLP-treated instruments in seven of the nine tests (77.8%, refer to Fig. 1). However, none of the reduction calculations met the American Society for Testing and Materials (ASTM) International passing criteria of 3 Log10 or 99.9%. In two of the nine tests (S1 and S5), increased bacterial growth occurred on the MicrobeCare XLP-treated forceps in comparison with the control forceps. Tests S3 and S4 included the shortest intervals for MicrobeCare XLP submersion and drying times (2 min each for two cycles) and did not undergo a second autoclave sterilization. Reduction calculations for these tests were the highest in the S. aureus groups, although they did not meet the specified requirements (S3 = 99.3% and S4 = 99.6%). Overall, the S. aureus untreated control forceps data set demonstrated particularly low concordance as depicted by Figure 2, with multiple extreme outlier values resulting in a mean (2.41 × 104) outside of the interquartile range. The mean colony count for the S. aureus MicrobeCare XLP-treated group was 8.56 × 103, compared with 2.41 × 104 for the control group; however, the difference was not statistically significant (p-value 0.109 by two-tailed unpaired two-sample t-test with unequal variance). Figure 2. View largeDownload slide S. aureus and A. baumannii colony counts on MicrobeCare XLP-treated and untreated control forceps. Figure 2. View largeDownload slide S. aureus and A. baumannii colony counts on MicrobeCare XLP-treated and untreated control forceps. In contrast, no growth of A. baumannii was observed on the MicrobeCare XLP-treated forceps in any of the tests performed. The overall minimum value in colony counts for the A. baumannii untreated control forcep group belonged to A6, which was the only series in the A. baumannii tests where the forceps underwent two autoclave treatments. The mean of the colony counts from the untreated control forceps was 7.28 × 103 across the six test series. All of the percent reduction calculations met the ASTM International passing criteria; the Log10 values could not be calculated. In addition, the difference between the means of the colony counts in the A. baumannii MicrobeCare XLP-treated forceps and untreated control forcep groups was statistically significant (p-value 0.008 by two-tailed unpaired two-sample t-test with unequal variance). Table I. S. aureus and A. baumannii Colony Counts on MicrobeCare XLP-treated and Untreated Control Forceps S. aureus  A. baumannii  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Treated forceps  Untreated control forceps  Percent (%)  Log10  Treated forceps  Untreated control forceps  Percent (%)  Log10  S1  2.51 × 104 (max)  3.70 × 103  −578.4  −0.8  A1  0  5.10 × 103  100.0  NA  S2  7.80 × 103  1.00 × 104  22.0  0.1  A2  0  1.44 × 104 (max)  100.0  NA  S3  1.20 × 102  1.66 × 104  99.3  2.1  A3  0  5.50 × 103  100.0  NA  S4  9.00 × 101 (min)  2.32 × 104  99.6  2.4  A4  0  9.70 × 103  100.0  NA  S5  9.20 × 103  1.80 × 103 (min)  −411.1  −0.7  A5  0  6.30 × 103  100.0  NA  S6  1.90 × 102  1.63 × 104  98.8  1.9  A6  0  2.70 × 103 (min)  100.0  NA  S7  9.00 × 103  4.90 × 104 (OL)  81.6  0.7            S8  8.50 × 103  1.65 × 104  48.5  0.3            S9  1.70 × 104  8.00 × 104 (max)  78.8  0.7            Median  8.50 × 103  1.65 × 104      Median  0  5.90 × 103      Mean  8.56 × 103  2.41 × 104      Mean  0  7.28 × 103      S. aureus  A. baumannii  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Treated forceps  Untreated control forceps  Percent (%)  Log10  Treated forceps  Untreated control forceps  Percent (%)  Log10  S1  2.51 × 104 (max)  3.70 × 103  −578.4  −0.8  A1  0  5.10 × 103  100.0  NA  S2  7.80 × 103  1.00 × 104  22.0  0.1  A2  0  1.44 × 104 (max)  100.0  NA  S3  1.20 × 102  1.66 × 104  99.3  2.1  A3  0  5.50 × 103  100.0  NA  S4  9.00 × 101 (min)  2.32 × 104  99.6  2.4  A4  0  9.70 × 103  100.0  NA  S5  9.20 × 103  1.80 × 103 (min)  −411.1  −0.7  A5  0  6.30 × 103  100.0  NA  S6  1.90 × 102  1.63 × 104  98.8  1.9  A6  0  2.70 × 103 (min)  100.0  NA  S7  9.00 × 103  4.90 × 104 (OL)  81.6  0.7            S8  8.50 × 103  1.65 × 104  48.5  0.3            S9  1.70 × 104  8.00 × 104 (max)  78.8  0.7            Median  8.50 × 103  1.65 × 104      Median  0  5.90 × 103      Mean  8.56 × 103  2.41 × 104      Mean  0  7.28 × 103      Table I. S. aureus and A. baumannii Colony Counts on MicrobeCare XLP-treated and Untreated Control Forceps S. aureus  A. baumannii  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Treated forceps  Untreated control forceps  Percent (%)  Log10  Treated forceps  Untreated control forceps  Percent (%)  Log10  S1  2.51 × 104 (max)  3.70 × 103  −578.4  −0.8  A1  0  5.10 × 103  100.0  NA  S2  7.80 × 103  1.00 × 104  22.0  0.1  A2  0  1.44 × 104 (max)  100.0  NA  S3  1.20 × 102  1.66 × 104  99.3  2.1  A3  0  5.50 × 103  100.0  NA  S4  9.00 × 101 (min)  2.32 × 104  99.6  2.4  A4  0  9.70 × 103  100.0  NA  S5  9.20 × 103  1.80 × 103 (min)  −411.1  −0.7  A5  0  6.30 × 103  100.0  NA  S6  1.90 × 102  1.63 × 104  98.8  1.9  A6  0  2.70 × 103 (min)  100.0  NA  S7  9.00 × 103  4.90 × 104 (OL)  81.6  0.7            S8  8.50 × 103  1.65 × 104  48.5  0.3            S9  1.70 × 104  8.00 × 104 (max)  78.8  0.7            Median  8.50 × 103  1.65 × 104      Median  0  5.90 × 103      Mean  8.56 × 103  2.41 × 104      Mean  0  7.28 × 103      S. aureus  A. baumannii  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Test series  Colony Counts (CFU/mL)  Reduction Calculations  Treated forceps  Untreated control forceps  Percent (%)  Log10  Treated forceps  Untreated control forceps  Percent (%)  Log10  S1  2.51 × 104 (max)  3.70 × 103  −578.4  −0.8  A1  0  5.10 × 103  100.0  NA  S2  7.80 × 103  1.00 × 104  22.0  0.1  A2  0  1.44 × 104 (max)  100.0  NA  S3  1.20 × 102  1.66 × 104  99.3  2.1  A3  0  5.50 × 103  100.0  NA  S4  9.00 × 101 (min)  2.32 × 104  99.6  2.4  A4  0  9.70 × 103  100.0  NA  S5  9.20 × 103  1.80 × 103 (min)  −411.1  −0.7  A5  0  6.30 × 103  100.0  NA  S6  1.90 × 102  1.63 × 104  98.8  1.9  A6  0  2.70 × 103 (min)  100.0  NA  S7  9.00 × 103  4.90 × 104 (OL)  81.6  0.7            S8  8.50 × 103  1.65 × 104  48.5  0.3            S9  1.70 × 104  8.00 × 104 (max)  78.8  0.7            Median  8.50 × 103  1.65 × 104      Median  0  5.90 × 103      Mean  8.56 × 103  2.41 × 104      Mean  0  7.28 × 103      DISCUSSION Antibacterial Efficacy Differing patterns of growth of S. aureus and A. baumannii were observed following treatment with MicrobeCare XLP in the testing sequences. S. aureus growth was particularly unpredictable: even test pairs that followed identical procedures (i.e., S8 and S9) demonstrated strikingly different results. Notably, growth of at least some S. aureus was detected on the MicrobeCare XLP-treated forceps in every test. Although some of the test series approached the ASTM guidelines for significance (in particular S3 and S4), none met or exceeded the requirements. The A. baumannii tests, in contrast, demonstrated no bacterial growth on the MicrobeCare XLP-treated forceps in any of the six tests performed. It is conceivable that differences in the cell wall structure between the gram-positive S. aureus and the gram-negative A. baumannii could account for these observed differences in MicrobeCare XLP’s efficacy. As discussed above, however, the mechanism of action of quaternary ammonium compounds remains unclear. Testing of other bacterial species would be necessary to draw a broader conclusion about whether or not MicrobeCare XLP is truly more effective at preventing gram-negative than gram-positive bacterial colonization. Logical bacteria to include in further testing could include Enterococcus faecium, Pseudomonas aeruginosa, and Enterobacter spp., which together (along with A. baumannii and S. aureus) compose the ESKAPE pathogens, a group of virulent bacteria that are responsible for the majority of nosocomial infections worldwide and commonly exhibit multi-drug antibiotic resistance.10,11 Influence of Repeat Autoclave Exposure In Tests S1 and S2 of the S. aureus experiments, the surgical forceps were subjected to a second sterilization via autoclave following the application of MicrobeCare XLP, which represented post-treatment bioload reduction. Surprisingly, Test S1 demonstrated a maximum value in colony counts among the MicrobeCare XLP-treated forceps exposed to S. aureus (2.51 × 104). Six of the other seven tests in which the forceps were only autoclaved before the MicrobeCare XLP application demonstrated higher bacterial counts from the untreated controls compared with the treated forceps. Tests S3 and S4 did not undergo a second autoclave sterilization and reduction calculations for these tests were the highest in the S. aureus groups (S3 = 99.3% and S4 = 99.6%). Although the reductions in microorganisms counts never reached the ASTM threshold for significance, these results suggested that MicrobeCare XLP was more effective against S. aureus after only a single autoclave sterilization. However, a similar decrease in efficacy was not observed in the A. baumannii test in which the forceps received two autoclave treatments (Test A6). This test also produced the overall minimum value in colony counts for the A. baumannii untreated control forceps group. We are therefore unable to definitively conclude that the additional autoclave exposure was the cause of the increased bacterial growth observed in the treatment group of S. aureus Tests S1, and the insignificant reduction of microorganisms in S2, based on these results alone. Additionally, the manufacturer offers data supporting the assertion that a MicrobeCare XLP coating can withstand a wide range of hospital-setting-cleansing practices such as routine terminal cleanings with a quaternary disinfectant,12 in addition to a variety of commonly used commercial disinfectant wipes and solutions including full-strength bleach.5 Given the inconsistencies between the manufacturer’s reports, the results obtained in our study, and historical data showing that QACs degrade over time,13 further testing is warranted to determine the efficacy of this product throughout different cleansing and sterilization procedures. Specifically, the addition of another commercially available disinfectant in a positive control group may be considered. Potential Impact of Post-exposure Bioload Reduction Although our group tested the MicrobeCare XLP product in a manner similar to other tests referenced in the product’s executive summary, we did not perform a bioload reduction step following pathogenic exposure as recommended. Our methodology specifically withheld this step as we were interested in the product’s use in resource-limited settings where post-exposure bioload reduction may be impractical or impossible. It is possible that the lack of bioload reduction following bacterial exposure limited the effectiveness of the product. This tertiary bioload reduction step may be incorporated into additional protocols to make a conclusion about its necessity and to represent typical clinical use. CONCLUSION During our evaluation of MicrobeCare XLP, we observed that the product was effective in preventing colonization by A. baumannii in several predetermined laboratory scenarios; the reduction in microorganisms between the treated and untreated control groups met both the ASTM International passing criteria and the traditional threshold of statistical significance. MicrobeCare XLP treatment did not lead to a statistically significant reduction of S. aureus by either calculation. Further testing of this product is warranted to fully evaluate its practical utility in a military operational environment. Additional studies could include a control group that undergoes post-exposure microbial load reduction, another disinfectant as a positive control, a wider range of health-care-associated pathogenic organisms, as well as other cleansing and sterilization processes. Funding Funding for this project was provided by the United States Air Force Clinical Investigator Program at the 59 Medical Wing at JBSA-Lackland, TX, and all laboratory evaluation was conducted at the 59th Clinical Research Division Laboratory at the 59th Medical Wing, JBSA-Lackland, TX. References 1 Rutala WA, Weber DJ, the Healthcare Infection Control Practices Advisory Committee (HICPAC). Guideline for disinfection and sterilization in healthcare facilities ( 2008). Centers for Disease Control and Prevention. https://www.cdc.gov/infectioncontrol/guidelines/Disinfection/index.html. Accessed October 26, 2017. 2 Merianos JJ: Surface-active agents. In: Disinfection, Sterilization, and Preservation , pp 283– 320. Edited by Block SS Philadelphia, PA, Lippincott Williams & Wilkins, 2001. 3 Petrocci AN: Surface active agents: quaternary ammonium compounds. In: Disinfection, Sterilization, and Preservation , pp 309– 29. Edited by Block SS, Philadelphia, PA, Lea & Febiger, 1983. 4 Asri LATW, Crismaru M, Roest S, Chen Y, Ivashenko O, Rudolf P, Tiller JC, van der Mei HC, Loontjens TJ A, Busscher HJ: A shape-adaptive, antibacterial-coating of immobilized quaternary-ammonium compounds tethered on hyperbranched polyurea and its mechanism of action. Adv Funct Mater  2014; 24: 346– 55. Google Scholar CrossRef Search ADS   5 Accelerated age testing with MicrobeCare with Ohio medical push to set suction regulators. MicrobeCareTM website. http://www.microbecare.com/wp-content/uploads/2015/10/Accelerated-Age-Testing-with-MicrobeCare.pdf. Accessed October 24, 2017. 6 Rutala WA, Cole EC: Ineffectiveness of hospital disinfectants against bacteria: a collaborative study. Infect Control  1987; 8: 501– 6. Google Scholar CrossRef Search ADS PubMed  7 Cole EC, Rutala WA, Samsa GP.: Disinfectant testing using a modified use-dilution method: collaborative study. J Assoc Off Anal Chem  1988; 71: 1187– 94. Google Scholar PubMed  8 Rutala WA, Cole EC, Wannamaker NS, Weber DJ: Inactivation of Mycobacterium tuberculosis and Mycobacterium bovis by 14 hospital disinfectants. Am J Med  1991; 91: 267S– 71S. Google Scholar CrossRef Search ADS PubMed  9 Jennings MC, Buttaro BA, Minbiole KPC, Wuest WM: Bioorganic investigation of multicationic antimicrobials to combat QAC-resistant Staphylococcus aureus. ACS Infect Dis  2015; 1( 7): 304– 9. Google Scholar CrossRef Search ADS PubMed  10 Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J: Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis  2009; 48( 1): 1– 12. Google Scholar CrossRef Search ADS PubMed  11 Santajit S, Indrawattana N: Mechanisms of antimicrobial resistance in ESKAPE pathogens. BioMed Res Int  2016; 2016: 2475067. Google Scholar CrossRef Search ADS PubMed  12 Lewis BD, Spencer M, Rossi PJ, Lee CJ, Brown KR, Malinowski M, Seabrook GR, Edmiston CE Jr: Assessment of an innovative antimicrobial surface disinfectant in the operating room environment using adenosine triphosphate bioluminescence assay. Am J Infect Control  2015; 43( 3): 283– 5. MicrobeCareTM website. http://www.microbecare.com/wp-content/uploads/2016/07/Lewis-et-al-2015-Am-J-Infection-Control.pdf. Accessed October 24, 2017. Google Scholar CrossRef Search ADS PubMed  13 Tezel U, Pavlostathis SG: Quaternary ammonium disinfectants: microbial adaptation, degradation and ecology. Curr Opin Biotechnol  2015; 33: 296– 304. Google Scholar CrossRef Search ADS PubMed  Author notes Opinions expressed are those of the authors and are not to be construed as official or as representing those of the U.S. Army, U.S. Air Force, the Department of Defense, or the U.S. Government. Mention of trade names, commercial products, or organizations does not imply endorsement by the U.S. Government. Published by Oxford University Press on behalf of the Association of Military Surgeons of the United States 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US.

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Military MedicineOxford University Press

Published: Apr 4, 2018

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