Advertisement

Cleaning and disinfection in home care: A comparison of 2 commercial products with potentially different consequences for respiratory health

Open AccessPublished:November 20, 2017DOI:https://doi.org/10.1016/j.ajic.2017.09.033

      Highlights

      • Describes the significance of cleaning and disinfection (C&D) work in home care and the importance of balancing infection prevention and respiratory health goals.
      • Evaluates the effectiveness of two C&D products—a bleach-containing product and an environmentally preferable product – for common household touch points in 46 homes.
      • Both products removed micro-organisms including Staphylococcus aureus from sampled surfaces.
      • Staphylococcus aureus was found in seven homes (out of 46) and Clostridium difficile in one home.
      • Additional research with other cleaning products and in more households is needed to develop robust recommendations for safe and effective C&D in home care.

      Background

      Home care aides perform personal care and homemaking services in client homes, including cleaning and disinfection (C&D). Although C&D are performed to remove soil and dust, they are increasingly performed for infection prevention. Many C&D products contain respiratory irritants. The objective of this study was to evaluate 2 commercial products for C&D effectiveness on common household surfaces in seniors' homes.

      Methods

      Two C&D visits were conducted in 46 seniors' homes. One visit applied a bleach-containing cleaning product and the other applied an environmentally preferable product. Before and after C&D, the study team performed organic soil bioluminometer measurements on surfaces and collected cotton swab and wipe samples for total bacteria count, Staphylococcus aureus, and Clostridium difficile identification.

      Results

      Both products removed microorganisms from tested surfaces. S aureus was found in 7 households, 1 strain of which was methicillin-resistant. Both products removed S aureus from all surfaces. Bleach-containing products removed somewhat more soil than environmentally preferable products, although results were statistically significant for only 1 surface.

      Conclusions

      The study showed similar, not identical, C&D performance for 2 cleaning products with potentially different consequences for respiratory health. Additional research is needed to develop robust recommendations for safe, effective C&D in home care.

      Key Words

      The rapidly aging US population and increasingly complex medical conditions managed at home demand more home-based providers for medical and social assistance care. Home care (HC) aides, who work in 1 of the fastest growing occupations in the United States, perform a wide range of services, including personal care of clients (such as showering and bathing) and homemaking, particularly cleaning and disinfection (C&D).
      • Markkanen P.
      • Quinn M.
      • Galligan C.
      • Sama S.
      • Brouillette N.
      • Okyere D.
      Characterizing the nature of home care work and occupational hazards: a developmental intervention study.
      • Quinn M.M.
      • Markkanen P.K.
      • Galligan C.J.
      • Sama S.R.
      • Kriebel D.
      • Gore R.J.
      • et al.
      Davis L. Occupational health of home care aides: results of the safe home care survey.
      Cleaning is a significant part of aides' work. In our recent survey in Massachusetts,
      • Quinn M.M.
      • Markkanen P.K.
      • Galligan C.J.
      • Sama S.R.
      • Kriebel D.
      • Gore R.J.
      • et al.
      Davis L. Occupational health of home care aides: results of the safe home care survey.
      we found that 80% of nearly 3,500 HC aide visits involved cleaning a bathroom or kitchen with 24% of visits involving bleach and an additional 23% involving ammonia or other strong chemical.
      Although cleaning tasks are performed to remove soil, dirt, and dust from home surfaces, they are also increasingly performed for infection prevention. One reason for the focus on disinfection is concern for infections in home health care
      • Shang J.
      • Larson E.
      • Liu J.
      • Stone P.
      Infection in home health care: results from national outcome and assessment information set data.
      and the rise in prevalence of drug-resistant pathogens, such as methicillin-resistant Staphylococcus aureus (MRSA) both in hospitals and in the community.
      • Goodyear N.
      • Brouillette N.
      • Tenaglia K.
      • Gore R.
      • Marshall J.
      The effectiveness of three home products in cleaning and disinfection of Staphylococcus aureus and Escherichia coli on home environmental surfaces.
      • Harrison E.M.
      • Ludden C.
      • Brodrick H.J.
      • Blane B.
      • Brennan G.
      • Morris D.
      • et al.
      Transmission of methicillin-resistant Staphylococcus aureus in long-term care facilities and their related healthcare networks.
      Clostridium difficile is the major cause of enteric infections among elderly persons.
      • Gould D.
      Prevention and control of Clostridium difficile infection.
      Patients returning home after exposures at facility-based health care settings can be carriers, which further compromises the health of home-based caregivers. Whereas cleaning removes soil, disinfection eliminates most recognized pathogenic microorganisms.
      • Goodyear N.
      • Brouillette N.
      • Tenaglia K.
      • Gore R.
      • Marshall J.
      The effectiveness of three home products in cleaning and disinfection of Staphylococcus aureus and Escherichia coli on home environmental surfaces.
      • U.S. Centers for Disease Control and Prevention
      Guide to Infection Prevention for Outpatient Settings: Minimum Expectations for Safe Care (Version 2.3).
      • Rutala W.
      • Weber D.
      Guideline for Disinfection and Sterilization in Healthcare Facilities.
      Increasingly, commercial products are formulated to accomplish C&D in 1 step. There are guidelines for C&D in hospitals and outpatient settings
      • U.S. Centers for Disease Control and Prevention
      Guide to Infection Prevention for Outpatient Settings: Minimum Expectations for Safe Care (Version 2.3).
      • Rutala W.
      • Weber D.
      Guideline for Disinfection and Sterilization in Healthcare Facilities.
      ; however, no guidelines exist for HC C&D.
      • Quinn M.M.
      • Henneberger P.K.
      Cleaning and disinfecting environmental surfaces in health care: toward an integrated framework for infection and occupational illness prevention.
      Complicating the choice of products to use for C&D, there is growing evidence that exposures to some common C&D products cause or exacerbate respiratory illnesses, including asthma and chronic bronchitis among janitors, domestic cleaners, and health care workers with regular exposure to cleaning products.
      • Quinn M.M.
      • Henneberger P.K.
      Cleaning and disinfecting environmental surfaces in health care: toward an integrated framework for infection and occupational illness prevention.
      • Delclos G.L.
      • Gimeno D.
      • Arif A.A.
      • Burau K.D.
      • Carson A.
      • Lusk C.
      • et al.
      Occupational risk factors and asthma among health care professionals.
      • Sastre J.
      • Madero M.F.
      • Fernandez-Nieto M.
      • Sastre B.
      • del Pozo V.
      • Potro M.G.
      • et al.
      Airway response to chlorine inhalation (bleach) among cleaning workers with and without bronchial hyperresponsiveness.
      • Delclos G.L.
      • Gimeno D.
      • Arif A.A.
      • Burau K.D.
      • Carson A.
      • Lusk C.
      • et al.
      Occupational risk factors and asthma among health care professionals.
      • Zock J.P.
      • Kogevinas M.
      • Sunyer J.
      • Almar E.
      • Muniozguren N.
      • Payo F.
      • et al.
      Asthma risk, cleaning activities and use of specific cleaning products among Spanish indoor cleaners.
      • Folletti I.
      • Siracusa A.
      • Paolocci G.
      Update on asthma and cleaning agents.
      • Dumas O.
      • Le Moual N.
      Do chronic workplace irritant exposures cause asthma?.
      • Matulonga B.
      • Rava M.
      • Siroux V.
      • Bernard A.
      • Dumas O.
      • Pin I.
      • et al.
      Women using bleach for home cleaning are at increased risk of non-allergic asthma.
      • Folletti I.
      • Zock J.P.
      • Moscato G.
      • Siracusa A.
      Asthma and rhinitis in cleaning workers: a systematic review of epidemiological studies.
      Indeed, cleaning products are among the leading causes of occupational asthma.
      • Arif A.A.
      • Delclos G.L.
      • Whitehead L.W.
      • Tortolero S.R.
      • Lee E.S.
      Occupational exposures associated with work-related asthma and work-related wheezing among U.S. workers.
      • Rosenman K.D.
      • Reilly M.J.
      • Schill D.P.
      • Valiante D.
      • Flattery J.
      • Harrison R.
      • et al.
      Cleaning products and work-related asthma.
      • Zock J.P.
      • Vizcaya D.
      • Le Moual N.
      Update on asthma and cleaners.
      Because of high volatility, spray application, and use in small and poorly ventilated spaces, there is concern that some C&D product exposures may be sufficient to increase respiratory illness risks among HC aides who clean and disinfect clients' homes. This may at least partially explain the finding that HC aides in Massachusetts had twice the prevalence of asthma compared with all other workers (20% vs 10%) in the Behavioral Risk Factor Surveillance Survey, 2011-2014.
      • Massachusetts Department of Public Health
      DataBrief: Occupational Lung Disease Bulletin.
      Concerns about adverse human and environmental health effects of C&D products have led to the development of so-called green cleaning products. In fact, there are several different terms used for these products by manufacturers, marketers, and environmental services professional groups, such as environmentally friendly, environmentally preferable, and green. It is important to note that there is still no accepted official definition of green. The 1998 US Executive Order 13101
      • The US Federal Register
      • The White House
      The President's Executive Order 13101—Greening the Government Through Waste Prevention, Recycling, and Federal Acquisition, Executive Order 13101.
      defined environmentally preferable as “products or services that have a lesser or reduced effect on human health and the environment when compared with competing products or services that serve the same purpose.” Despite the fact that there is no standard definition for the general concept of green, including a green cleaning product, this sector of the consumer products market is rapidly growing and some hospitals and other institutions have adopted initiatives such as green cleaning programs. Based on toxicologic screenings, there is limited evidence on how green cleaning products influence human health. Additionally, little is known about whether green cleaning products are as effective as conventional products for disinfecting as well as for cleaning in actual home and health care settings.
      • Goodyear N.
      • Brouillette N.
      • Tenaglia K.
      • Gore R.
      • Marshall J.
      The effectiveness of three home products in cleaning and disinfection of Staphylococcus aureus and Escherichia coli on home environmental surfaces.
      • Quinn M.M.
      • Henneberger P.K.
      Cleaning and disinfecting environmental surfaces in health care: toward an integrated framework for infection and occupational illness prevention.
      The American Society for Healthcare Environmental Services has recommended
      • Beaver M.
      Healthcare facilities hesitantly embrace green cleaning principles and products. Infection Control Today (May 31, 2007).
      that the green cleaning definition be expanded to address the efficacy of infection control and prevention “towards effective products with the fewest adverse effects on human health and the environment.”
      The objective of our study was to evaluate the effectiveness of alternative commercial products for C&D of common household touch points under conditions typical of a visit by an HC aide in the homes of residents in senior housing complexes. Two commonly available products were compared, a conventional cleaner containing chlorine bleach, and another marketed as green. For the purposes of this article, environmentally preferable will be used rather than green. The study was informed by a laboratory investigation that tested 3 products for C&D efficacy under controlled conditions with known sample contamination, including the 2 products used in this field study
      • Goodyear N.
      • Brouillette N.
      • Tenaglia K.
      • Gore R.
      • Marshall J.
      The effectiveness of three home products in cleaning and disinfection of Staphylococcus aureus and Escherichia coli on home environmental surfaces.
      and a qualitative investigation of 9 focus groups of HC aides and 7 in-depth interviews with HC managers to characterize HC C&D practices and products so that these could be applied in the present study. The findings of the qualitative study will be reported elsewhere.

      Methods

      The sampling and culture methods of this study are based on previously published literature.
      • Cataldo M.C.
      • Bonura C.
      • Caputo G.
      • Aleo A.
      • Rizzo G.
      • Geraci D.M.
      • et al.
      Colonization of pressure ulcers by multidrug-resistant microorganisms in patients receiving home care.
      • Scott E.
      • Duty S.
      • McCue K.
      A critical evaluation of methicillin-resistant Staphylococcus aureus and other bacteria of medical interest on commonly touched household surfaces in relation to household demographics.
      • Uhlemann A.C.
      • Knox J.
      • Miller M.
      • Hafer C.
      • Vasquez G.
      • Ryan M.
      • et al.
      The environment as an unrecognized reservoir for community-associated methicillin resistant Staphylococcus aureus USA300: a case-control study.
      • Weese J.S.
      • Finley R.
      • Reid-Smith R.R.
      • Janecko N.
      • Rousseau J.
      Evaluation of Clostridium difficile in dogs and the household environment.
      • Alam M.J.
      • Anu A.
      • Walk S.T.
      • Garey K.W.
      Investigation of potentially pathogenic Clostridium difficile contamination in household environs.
      The study was approved by the University of Massachusetts Lowell Institutional Review Board. All participants signed an informed consent form. Three local senior housing complexes in Massachusetts were recruited as research study sites. With the assistance of the housing authorities, our study team recruited and visited 46 homes between January and September 2016.
      A team of 3 researchers conducted 2 visits at each home, at least 1 week apart. During 1 visit, a bleach-containing (BC) product was used (Clorox Cleanup Cleaner + Bleach; The Clorox Company, Oakland, CA) and the other visit tested an environmentally preferable (EP) product (Seventh Generation Disinfecting Multi-Surface Cleaner; Seventh Generation Inc, Burlington, VT). The research team members have no relationship with the manufacturers of these products. The cleaning products were purchased at a local grocery store. The BC product was selected based on input from HC aides who participated in focus groups to identify commonly used C&D products. HC aides reported very infrequent use of green products and the EP product selected for this study was based on common availability in grocery stores. The efficacy of these 2 products was evaluated in an earlier laboratory pilot investigation, which has been reported elsewhere.
      • Goodyear N.
      • Brouillette N.
      • Tenaglia K.
      • Gore R.
      • Marshall J.
      The effectiveness of three home products in cleaning and disinfection of Staphylococcus aureus and Escherichia coli on home environmental surfaces.
      Residents were not told the names of the products or which type was applied during a visit. The order of product use (first visit vs second visit) was randomized.
      Residents received a $40 cash incentive for the first visit and $60 for the second visit. A study visit lasted no more than 45 minutes. The team members wore disposable shoe covers during the entire study visit to protect residents' floors as well as gloves during sampling and cleaning to protect samples from hand contamination. Eight high-touch surfaces were sampled in each home: 4 surfaces in the kitchen (sink, counter, floor, and faucet) and 4 surfaces in the bathroom (tub or shower, toilet seat, floor, and faucet). Analyses included rapid measurements of organic soil (hereafter called soil), including bacteria, food residue, and human cells using an ATP luminometer (SystemSure Plus, Hygiena, Camarillo, CA); total aerobic plate counts (TAPC) as a measure of overall bacterial contamination and disinfection effectiveness; the presence of S aureus, differentiating MRSA and methicillin-susceptible S aureus (MSSA) strains after isolation, as an indicator of a significant pathogen; and the presence of C difficile, differentiating nontoxigenic and toxigenic strains.
      The bathroom and kitchen faucets were sampled for TAPC and S aureus only, by rubbing the entire surface of the handle with a sterile swab premoistened with D/E Neutralization Broth (Becton, Dickinson and Company, Franklin Lakes, NJ) to stop the activity of any residual disinfectant.
      The toilet seat and bathroom floor next to the toilet were sampled for C difficile only, using Swiffer Sweeper dry cloths (Procter & Gamble, Cincinnati, OH), which pick up dust and soil electrostatically.
      • Weese J.S.
      • Finley R.
      • Reid-Smith R.R.
      • Janecko N.
      • Rousseau J.
      Evaluation of Clostridium difficile in dogs and the household environment.
      The toilet seat was split into left and right sides and 1 entire side was wiped before and after cleaning. The floor next to the toilet was sampled using a template with 20 cm × 20 cm (400 cm2 in total) sampling areas, 1 for precleaning and 1 for postcleaning. The entire template area was wiped with a Swiffer cloth.
      The kitchen floor, counter, sink, and bathroom tub or shower were sampled for ATP, TAPC, and S aureus. A 4-section sampling template was used to define the sample area (20 × 20 cm), with separate areas for ATP and swab sampling, as well as precleaning and postcleaning. ATP luminometer measurements were performed using Ultrasnap ATP Test swabs (Hygiena) following the manufacturer's instructions. Sterile swabs, premoistened in D/E Broth were used for TAPC and S aureus sampling.
      After all precleaning samples were taken, a brief spot cleaning was performed on all surfaces: cleaning product was sprayed directly on the surface and wiped immediately with a paper towel, to model actual home cleaning methods. After 10 minutes to allow the product to dry, postcleaning samples were taken. After sampling, swabs were placed in 1 mL D/E Neutralization Broth, Swiffers were sealed in plastic bags, and all were transported on ice to the microbiology laboratory for culture. All samples were processed within 24 hours of collection. One study visit produced 16 precleaning and postcleaning samples in total.

      TAPC

      TAPC methods are based on previously published literature.
      • Scott E.
      • Duty S.
      • McCue K.
      A critical evaluation of methicillin-resistant Staphylococcus aureus and other bacteria of medical interest on commonly touched household surfaces in relation to household demographics.
      In the laboratory, TAPC were performed from the neutralizing broth in which swabs were transported. After vortex mixing for 10 seconds, serial 10-fold dilutions were made using phosphate-buffered saline and 100 µL was spread plated to duplicate tryptic soy agar plates (Becton, Dickinson and Company, Franklin Lakes, NJ) and incubated overnight at 37°C. Recovered colonies were visually inspected and counted.

      S aureus screening

      S aureus screening methods are based on previously published literature.
      • Cataldo M.C.
      • Bonura C.
      • Caputo G.
      • Aleo A.
      • Rizzo G.
      • Geraci D.M.
      • et al.
      Colonization of pressure ulcers by multidrug-resistant microorganisms in patients receiving home care.
      • Scott E.
      • Duty S.
      • McCue K.
      A critical evaluation of methicillin-resistant Staphylococcus aureus and other bacteria of medical interest on commonly touched household surfaces in relation to household demographics.
      • Uhlemann A.-C.
      • Knox J.
      • Miller M.
      • Hafer C.
      • Vasquez G.
      • Ryan M.
      • et al.
      The environment as an unrecognized reservoir for community-associated methicillin resistant Staphylococcus aureus USA300: a case-control study.
      A 100-µL aliquot of the original neutralization broth was spread plated to duplicate mannitol salt agar plates (Becton, Dickinson and Company) and incubated overnight at 37°C. If growth was absent or insufficient, plates were reincubated for another 24 hours before final interpretation. In addition, the original swabs were placed in 3 mL Staphylococcus Broth (Becton, Dickinson and Company) and incubated at 37°C for 48 hours. Following incubation, a 100-µL aliquot of Staphylococcus Broth was inoculated in duplicate onto mannitol salt agar and incubated at 37°C overnight, with an additional 24 hours' incubation if growth was absent or minimal. Suspected S aureus colonies were identified by Gram stain, catalase test, and the Sure-Vue SELECT Staph ID Latex Slide Agglutination Test (Fisher Healthcare, Waltham, MA). Methicillin-resistant isolates were screened and confirmed using the PBP2a SA Culture Colony Test (Alere Inc, Waltham, MA).

      C difficile screening

      C difficile screening methods are based on previously published literature.
      • Alam M.J.
      • Anu A.
      • Walk S.T.
      • Garey K.W.
      Investigation of potentially pathogenic Clostridium difficile contamination in household environs.
      Phosphate-buffered saline (25 mL) was added to the sterile collection bag containing the Swiffer cloths. The bags were homogenized manually for approximately 1 minute by squeezing vigorously. This solution was inoculated in 25 mL tryptic soy broth (Becton, Dickinson, and Company) and incubated at 37°C for 48 hours. After incubation, broths were subjected to alcohol shock by adding 1 mL tryptic soy broth to 1 mL absolute ethanol. The mixture was incubated at room temperature for 1 hour and vortex mixed every 10 to 15 minutes. After treatment, 100 µL of the mixture was inoculated onto prereduced tryptic soy broth with 5% sheep blood agar (SBA) and C difficile selective agar (both from Becton, Dickinson and Company) and incubated anaerobically for 48 hours, with an additional 48-hour incubation for plates with no or minimal growth. Colonies on C difficile selective agar and SBA consistent with typical C difficile morphology were subcultured to SBA, and their identification was confirmed through Gram stain and the C. diff Quik Chek Complete Antigen Test (Alere Inc).

      Data analysis

      Paired differences were used to calculate the change in precleaning minus postcleaning levels for both ATP readings and log10 TAPC. Thus, positive values represent decreases in mean levels, indicating that the treatment reduced soil or bacteria, respectively. Pairing was done by sampling site within a home visit. Paired differences of pre–post change within a home by sampling site were calculated to represent the comparative efficacy of the BC product compared with the EP product. Thus a positive difference indicated that the BC product was more effective than the EP product. Box plots
      • Tukey J.W.
      Exploratory Data Anaylsis. Reading (MA): Addison-Wesley Publishing Company.
      were produced for both ATP measurements and log10 TAPC by site and by cleaning product. All calculations were performed using SAS version 9.4 software for Windows (SAS Institute Inc, Cary NC).

      Results

      Population characteristics

      Measurements were completed in 46 households (Table 1). Forty-five households had a single resident who enrolled as the study participant. One household had 2 adult residents; however, only 1 member of this household was registered as the study participant. The age range of participants was 46-95 years, average age was 75 years, and median age was 77.5 years. Most participants were women (76%), and only 1 resident self-identified as nonwhite. Ten participating households (22%) had pets (7 cats, 1 dog, and 2 birds); 14 households (30%) received some type of HC services, including homemaking assistance; and 5 households (11%) received other cleaning services. Seven participants had had an overnight hospitalization during the 3 months before the study visit.
      Table 1Household characteristics in a cleaning and disinfection in home care study, January-September 2016
      All participating households (n = 46)n%
      Household makeup
       1-person households4598
       2-person households
      Only 1 member of this household participated in the study.
      12
      Gender of the household participant
       Female3576
       Male1124
      Age of household participant, y
        < 5012
       50-691431
       70-892861
        ≥ 9037
      Households with pets1022
      Households receiving home care services1430
      Household receiving cleaning services511
      Hospitalization within 3 mo715
      * Only 1 member of this household participated in the study.

      ATP bioluminescence

      An ATP luminometer was used to measure organic soil on specific household surfaces in relative light units (RLUs) of bioluminescence per 400 cm2 in each household before and after cleaning with each product (Table 2 and Fig 1). Precleaning, the highest average soil levels were found in the kitchen sink (1,718 RLU/400 cm2 from the BC product sample sites and 1,752 from the EP product sample sites). The other 3 sample sites, kitchen counter, bathroom tub/shower, and kitchen floor had considerably less organic soil on average before the study cleaning began. Of the 4 sampling sites, in only 1—the tub—was the pre–post reduction significantly larger (ie, more clean) using the BC product compared with the EP product (Table 2). There was wide variability in soil levels among the samples, notably for the tub and kitchen sink (Fig 1).
      Table 2Comparison of cleaning effectiveness
      Organic soil levels measured as ATP relative light units of bioluminescence/400 cm2 of a specific household surface.
      of a bleach-containing (BC) versus an environmentally preferable (EP) product applied in senior housing, January-September 2016
      BC productEP productBC – EP
      Difference in mean pre–post cleaning change, comparing BC with EP products.
      Sampling site (N = 46)Pre- cleaning averagePost- cleaning averageMean changePre-cleaning averagePost- cleaning averageMean changeMean (95% confidence interval)
      Bathroom tub (n = 46)7455868739829998589 (27 to 1,150)
      Kitchen counter (n = 46)55084465602289313152 (−141 to 447)
      Kitchen floor (n = 46)5027143159617741813 (−175 to 200)
      Kitchen sink (n = 46)171888283617571378379458 (−486 to 1,402)
      * Organic soil levels measured as ATP relative light units of bioluminescence/400 cm2 of a specific household surface.
      Difference in mean pre–post cleaning change, comparing BC with EP products.
      Fig 1
      Fig 1Box plot comparison of organic soil levels comparing bleach-containing (BC) versus environmentally preferable (EP) cleaning products applied in senior housing, January-September 2016. Organic soil levels were measured as ATP relative light units of bioluminescence/400 cm2 of specific household surface.

      TAPC

      Both products reduced the TAPC of microorganisms on all surfaces (Fig 2). The BC product achieved an overall average 2.26 log10 reduction on all surfaces (range, 2.20-2.74 log10) and the EP product achieved an overall average reduction of 1.65 log10 (range, 1.42-1.84 log10). These reductions correspond to 90% or better reductions in median TAPC using either product.
      Fig 2
      Fig 2Total precleaning and postcleaning results for bleach-containing (BC) product versus environmentally preferable (EP) product applied in senior housing, January-September 2016. TAPC, total aerobic plate counts.
      There were 24 sampling site pairs where neither precleaning nor postcleaning samples had any bacterial growth, and 50 sampling site pairs (9%) where 1 reading (pre or post) was above the limit of detection. In these 74 cases, TAPC reduction calculations could not be performed. This occurred most frequently with the kitchen sink, with 19 instances (38%) followed by 10 for the tub or shower (20%), 6 each for the kitchen counter and kitchen floor (2%), 5 for the bathroom faucet (10%), and 4 for the kitchen faucet (8%).

      Identification of S aureus and C difficile

      There were only 7 households in which S aureus was found—6 MSSA and 1 MRSA strain (Table 3). Kitchen surfaces, in particular the kitchen sink, were the most common surfaces where S aureus was found. All MSSA and MRSA were identified precleaning only; no S aureus was identified in any postcleaning sample. Both products removed S aureus from all surfaces sampled. C difficile was found in only 1 household visit, on the toilet seat, in both precleaning and postcleaning samples. In this household, C difficile was found in only 1 of the 2 visits. Two of the 8 households where either S aureus or C difficile was found received HC services.
      Table 3Identification of Staphylococcus aureus pathogens in precleaning samples. Pathogens were not found in any postcleaning samples collected in senior housing units, January-September 2016
      Household visitedPathogen foundSampling sites where pathogen was found
      1MSSAKitchen sink, counter and floor
      2MSSAKitchen sink
      3MSSAKitchen sink
      4MSSABathroom tub
      5MSSAKitchen counter
      6MSSAKitchen sink
      7MRSAKitchen sink
      MRSA, methicillin resistant Staphylococcus aureus; MSSA, methicillin susceptible Staphylococcus aureus.

      Discussion

      Soil, measured by ATP RLUs

      Both cleaning products removed organic soil on all tested surfaces, based on the study precleaning and postcleaning ATP luminometer measurements. ATP levels reflect the presence of organic material such as living cells and cellular material that is no longer viable, but not inorganic soils (eg, sand or dust). Overall, we found that the BC product removed somewhat more organic soil than the EP product, although the difference was modest and statistically significant at only 1 sampling site. The ATP luminometer is used in foodservice and commercial facilities to monitor general cleaning effectiveness and for training purposes. There are no guidelines or targets for what levels constitute clean enough for home cleaning. Thus it is difficult to judge the health influence of the modest differences we observed between products.
      We designed the study's cleaning protocol to model what is typically done in actual home cleaning rather than following the manufacturers' instructions, which recommend leaving the EP product on the surface for 10 minutes before wiping it off. The shorter contact time may have reduced the effectiveness of the EP product. Our previous pilot study in a laboratory setting showed that this same EP product, when used as directed, worked as effectively as the BC product for cleaning and disinfecting a stainless steel surface, and when disinfecting a ceramic surface.
      • Goodyear N.
      • Brouillette N.
      • Tenaglia K.
      • Gore R.
      • Marshall J.
      The effectiveness of three home products in cleaning and disinfection of Staphylococcus aureus and Escherichia coli on home environmental surfaces.
      In this study overall, the kitchen sink surface had the most organic soil and was the hardest to clean; neither product achieved a 50% or greater reduction in RLUs/400 cm2 readings. The area around the drain, where sampling occurred, can be difficult to access and the stainless steel surface may become scratched over time, allowing microorganisms and food residue to remain. In addition, the sink is a wet surface, which may support organisms better than the dry floor and counter surfaces. The bathtub or shower, also a frequently wet surface, had the second highest maximum readings, although the means were similar to the kitchen counter and floor. The BC product performed best on the bathtub or shower, whereas the EP product performed best on the floor.

      TAPC

      A real-world evaluation of the effectiveness of disinfectants is necessarily limited by the presence of microorganisms before cleaning—if the concentrations are low, it is not possible to observe a large reduction in counts regardless of the product. The participants of this study were asked to not clean the kitchen and bathroom surfaces for 2 days before the team's sampling and cleaning visit, and at the start of each visit, the participants were asked to confirm this. Nonetheless, in our study not all sampled surfaces had precleaning TAPC of microorganisms ≥3.00 log10. The 3.00 log10 TAPC reduction meets the Environmental Protection Agency standard for nonfood contact surface disinfection requirement; that is, the commonly accepted threshold defining disinfection.
      • Environmental Protection Agency
      • Office of Pesticide Programs
      Sanitizer test for inanimate surfaces.
      In this study's 160 complete sampling pairs, where the precleaning TAPC was ≥3.00 log10, the BC product achieved at least a 3.00 log10 reduction 52 times and EP product 18 times. No guidelines exist for home environment disinfection effectiveness.
      When our study sampling pairs are expressed as percent reduction in TAPC, the BC product achieved an overall median microorganism reduction of 100% and the EP product achieved a 99% reduction. For the general population without extensive knowledge in microbiology, percent TAPC reductions are a more understandable disinfection effectiveness concept than log10 reductions.
      Our previous lab study
      • Goodyear N.
      • Brouillette N.
      • Tenaglia K.
      • Gore R.
      • Marshall J.
      The effectiveness of three home products in cleaning and disinfection of Staphylococcus aureus and Escherichia coli on home environmental surfaces.
      showed that with a 30-second wet contact time, the BC and EP products were equally effective at killing Escherichia coli and MSSA organisms (≥5 log10 reduction) on common household surfaces dosed with these common bacteria.

      C difficile, MRSA, and MSSA

      C difficile was found only in 1 home and MRSA in 1 other home. MSSA was found in about 6% of visits. As mentioned, 2 of the 8 households where these pathogens were found received HC services. Pets, cleaning services, and overnight hospitalizations had either no or very minimal association in identification of these organisms; however, the study population was relatively small and with a larger sample size an association could have been possible. The prevalences of these pathogens were lower than other researchers have reported for home-based studies. Scott et al
      • Scott E.
      • Duty S.
      • McCue K.
      A critical evaluation of methicillin-resistant Staphylococcus aureus and other bacteria of medical interest on commonly touched household surfaces in relation to household demographics.
      studied a sample of 35 random homes in the Boston metropolitan area and collected wipe samples from 32 surfaces in each. MRSA was found in 26% of these homes, and MSSA was found in all but 1 of the homes. In comparison to our study, Scott et al
      • Scott E.
      • Duty S.
      • McCue K.
      A critical evaluation of methicillin-resistant Staphylococcus aureus and other bacteria of medical interest on commonly touched household surfaces in relation to household demographics.
      sampled more surfaces, including dish cloths and sponges, toys, pet food dishes, and others.
      • Scott E.
      • Duty S.
      • McCue K.
      A critical evaluation of methicillin-resistant Staphylococcus aureus and other bacteria of medical interest on commonly touched household surfaces in relation to household demographics.
      Alam et al
      • Alam M.J.
      • Anu A.
      • Walk S.T.
      • Garey K.W.
      Investigation of potentially pathogenic Clostridium difficile contamination in household environs.
      found C difficile in 32% of 30 Houston area homes, with greatest prevalence from shoe bottom swab samples (40%), bathroom or toilet surfaces (33%), and house floor dust (33%). A possible explanation is that all but 1 of the 46 households participating in our study had only 1 resident and all residents were adults, many with limited mobility and thus with limited opportunities for transporting soil and microorganisms from the outside environment into the home.

      Conclusions

      C&D of environmental surfaces are key components of infection prevention in health care, including at home. This study found similar, but not identical performance of C&D for 2 different cleaning products with potentially different consequences for respiratory health. We encourage additional research with other cleaning products and in a larger number of homes to develop a more robust database for recommendations of safe and effective C&D in HC settings.

      Acknowledgments

      The authors thank Noor Sheikh for assisting with sampling of the household surfaces. The authors also thank the 3 housing agencies, the household residents, and especially all home care aides in the United States.

      References

        • Markkanen P.
        • Quinn M.
        • Galligan C.
        • Sama S.
        • Brouillette N.
        • Okyere D.
        Characterizing the nature of home care work and occupational hazards: a developmental intervention study.
        Am J Ind Med. 2014; 57: 445-457
        • Quinn M.M.
        • Markkanen P.K.
        • Galligan C.J.
        • Sama S.R.
        • Kriebel D.
        • Gore R.J.
        • et al.
        Davis L. Occupational health of home care aides: results of the safe home care survey.
        Occup Environ Med. 2016; 73: 237-245
        • Shang J.
        • Larson E.
        • Liu J.
        • Stone P.
        Infection in home health care: results from national outcome and assessment information set data.
        Am J Infect Control. 2015; 43: 454-459
        • Goodyear N.
        • Brouillette N.
        • Tenaglia K.
        • Gore R.
        • Marshall J.
        The effectiveness of three home products in cleaning and disinfection of Staphylococcus aureus and Escherichia coli on home environmental surfaces.
        J Appl Microbiol. 2015; 119: 1245-1252
        • Harrison E.M.
        • Ludden C.
        • Brodrick H.J.
        • Blane B.
        • Brennan G.
        • Morris D.
        • et al.
        Transmission of methicillin-resistant Staphylococcus aureus in long-term care facilities and their related healthcare networks.
        Genome Med. 2016; 8: 102
        • Gould D.
        Prevention and control of Clostridium difficile infection.
        Nurs Older People. 2010; 22 (quiz 5): 29-34
        • U.S. Centers for Disease Control and Prevention
        Guide to Infection Prevention for Outpatient Settings: Minimum Expectations for Safe Care (Version 2.3).
        (National Center for Emerging and Zoonotic Infectious Diseases; Available from:)
        https://www.cdc.gov/infectioncontrol/pdf/outpatient/guide.pdf
        Date: 2016
        Date accessed: September 26, 2017
        • Rutala W.
        • Weber D.
        Guideline for Disinfection and Sterilization in Healthcare Facilities.
        (The Healthcare Infection Control Practices Advisory Committee (HICPAC). US Department of Health and Human Services, Centers for Disease Control and Prevention (CDC); Available from:)
        • Quinn M.M.
        • Henneberger P.K.
        Cleaning and disinfecting environmental surfaces in health care: toward an integrated framework for infection and occupational illness prevention.
        Am J Infect Control. 2015; 43: 424-434
        • Delclos G.L.
        • Gimeno D.
        • Arif A.A.
        • Burau K.D.
        • Carson A.
        • Lusk C.
        • et al.
        Occupational risk factors and asthma among health care professionals.
        Am J Respir Crit Care Med. 2007; 175: 667-675
        • Sastre J.
        • Madero M.F.
        • Fernandez-Nieto M.
        • Sastre B.
        • del Pozo V.
        • Potro M.G.
        • et al.
        Airway response to chlorine inhalation (bleach) among cleaning workers with and without bronchial hyperresponsiveness.
        Am J Ind Med. 2011; 54: 293-299
        • Delclos G.L.
        • Gimeno D.
        • Arif A.A.
        • Burau K.D.
        • Carson A.
        • Lusk C.
        • et al.
        Occupational risk factors and asthma among health care professionals.
        Am J Respir Crit Care Med. 2007; 175: 667-675
        • Zock J.P.
        • Kogevinas M.
        • Sunyer J.
        • Almar E.
        • Muniozguren N.
        • Payo F.
        • et al.
        Asthma risk, cleaning activities and use of specific cleaning products among Spanish indoor cleaners.
        Scand J Work Environ Health. 2001; 27: 76-81
        • Folletti I.
        • Siracusa A.
        • Paolocci G.
        Update on asthma and cleaning agents.
        Curr Opin Allergy Clin Immunol. 2017; 17: 90-95
        • Dumas O.
        • Le Moual N.
        Do chronic workplace irritant exposures cause asthma?.
        Curr Opin Allergy Clin Immunol. 2016; 16: 75-85
        • Matulonga B.
        • Rava M.
        • Siroux V.
        • Bernard A.
        • Dumas O.
        • Pin I.
        • et al.
        Women using bleach for home cleaning are at increased risk of non-allergic asthma.
        Respir Med. 2016; 117: 264-271
        • Folletti I.
        • Zock J.P.
        • Moscato G.
        • Siracusa A.
        Asthma and rhinitis in cleaning workers: a systematic review of epidemiological studies.
        J Asthma. 2014; 51: 18-28
        • Arif A.A.
        • Delclos G.L.
        • Whitehead L.W.
        • Tortolero S.R.
        • Lee E.S.
        Occupational exposures associated with work-related asthma and work-related wheezing among U.S. workers.
        Am J Ind Med. 2003; 44: 368-376
        • Rosenman K.D.
        • Reilly M.J.
        • Schill D.P.
        • Valiante D.
        • Flattery J.
        • Harrison R.
        • et al.
        Cleaning products and work-related asthma.
        J Occup Environ Med. 2003; 45: 556-563
        • Zock J.P.
        • Vizcaya D.
        • Le Moual N.
        Update on asthma and cleaners.
        Curr Opin Allergy Clin Immunol. 2010; 10: 114-120
        • Massachusetts Department of Public Health
        DataBrief: Occupational Lung Disease Bulletin.
        (Asthma in Massachusetts Home Care Aides; Available from:)
        • The US Federal Register
        • The White House
        The President's Executive Order 13101—Greening the Government Through Waste Prevention, Recycling, and Federal Acquisition, Executive Order 13101.
        (Available from:)
        • Beaver M.
        Healthcare facilities hesitantly embrace green cleaning principles and products. Infection Control Today (May 31, 2007).
        (Available from:)
        • Cataldo M.C.
        • Bonura C.
        • Caputo G.
        • Aleo A.
        • Rizzo G.
        • Geraci D.M.
        • et al.
        Colonization of pressure ulcers by multidrug-resistant microorganisms in patients receiving home care.
        Scand J Infect Dis. 2011; 43: 947-952
        • Scott E.
        • Duty S.
        • McCue K.
        A critical evaluation of methicillin-resistant Staphylococcus aureus and other bacteria of medical interest on commonly touched household surfaces in relation to household demographics.
        Am J Infect Control. 2009; 37: 447-453
        • Uhlemann A.C.
        • Knox J.
        • Miller M.
        • Hafer C.
        • Vasquez G.
        • Ryan M.
        • et al.
        The environment as an unrecognized reservoir for community-associated methicillin resistant Staphylococcus aureus USA300: a case-control study.
        PLoS ONE. 2011; 6 (e22407)
        • Weese J.S.
        • Finley R.
        • Reid-Smith R.R.
        • Janecko N.
        • Rousseau J.
        Evaluation of Clostridium difficile in dogs and the household environment.
        Epidemiol Infect. 2010; 138: 1100-1104
        • Alam M.J.
        • Anu A.
        • Walk S.T.
        • Garey K.W.
        Investigation of potentially pathogenic Clostridium difficile contamination in household environs.
        Anaerobe. 2014; 27: 31-33
        • Uhlemann A.-C.
        • Knox J.
        • Miller M.
        • Hafer C.
        • Vasquez G.
        • Ryan M.
        • et al.
        The environment as an unrecognized reservoir for community-associated methicillin resistant Staphylococcus aureus USA300: a case-control study.
        PLoS ONE. 2011; 6: e22407
        • Tukey J.W.
        Exploratory Data Anaylsis. Reading (MA): Addison-Wesley Publishing Company.
        1977
        • Environmental Protection Agency
        • Office of Pesticide Programs
        Sanitizer test for inanimate surfaces.
        (DIS/TSS-10; Available at:)
        https://archive.epa.gov/pesticides/oppad001/web/html/dis-10.html
        Date: 1976
        Date accessed: September 26, 2017