Discussion

This study showed [1] the feasibility of using an ATP bioluminescence assay in ambulatory settings to monitor cleanliness of environmental surfaces and equipment. All sites had excellent adherence to the study protocol as indicated by complete sampling rates. Overall, the mean pass rates for all tested surfaces, at all rounds, at all study sites were 75%–80%; [2] certain surfaces (BP equipment) were more likely to pass whereas the exam room chair in pediatric clinics had the lowest pass rates compared to other surfaces even after feedback. Further this study showed that [3] the pass rates were higher in adult clinics than in pediatric clinics. Based on improved pass rates with cleaning (R3) with further improvement in R5 for certain surfaces in the pediatric clinics (Figure 2), cleaning and feedback appeared to be helpful. Improvements also differed by surfaces; the highest pass-rates for the front desk, exam room table and chair occurred at R5.

The higher rate of contamination in pediatric clinics may be explained by more frequent touching of surroundings and less frequent hand hygiene performed by young patients and potentially their accompanying siblings. Besides clinic spaces passing more often in the adult compared to pediatric clinics there were differences by surface that we can only speculative on. The BP equipment was “cleanest” which may be due to it’s easy to clean flat surface and that the person who is in direct patient contact wipes it down immediately after use. On the other hand, key-boards in the exam room may be more difficult to remember after a visit and in pediatric clinics children often play with it. Interestingly, the Front desk/Check in surface showed marked improvement after feedback which may be due to this surface not receiving attention at baseline.

Contaminated surfaces can serve as reservoirs for pathogens causing healthcare-associated infections in both CF and non-CF populations as supported by epidemiologic studies and experimental data. ^{Reference Hota8–Reference Kuczewski, Henaff and Regard12} In CF clinics, potential pathogens can survive on sinks, tables, toys, and chairs for extended periods. ^{Reference Festini, Buzzetti and Bassi13,Reference Zimakoff, Hoiby and Rosendal14} Transmission of Pseudomonas aeruginosa within CF care centers has been documented in many countries, ^{Reference Kidd, Ramsay and Hu15,Reference Stapleton, Izydorcyzk and Clark16} with fewer shared strains after implementation of stricter IP&C measures. ^{Reference Hoiby and Pedersen17,Reference Wiehlmann, Cramer and Ulrich18} However, we could only find one prior study that addressed strategies to reduce the potential risk posed by contaminated surfaces in CF clinics. Using agar contact plates to quantify bacterial burden before cleaning, the highest colony forming units (CFUs) were noted in and around sinks, and on exam room chairs and desks. ^{Reference Allen, Jadkauskaite and Shafi19} Following manual cleaning, CFUs were significantly reduced for most surfaces. While the study found that ultraviolet (UV) lights further reduced CFUs on all surfaces, UV disinfection can adversely affect clinic flow due to the time required, UV lights are costly to maintain, and are not currently recommended for CF care settings. ^{Reference Saiman, Siegel and LiPuma1}

ATP testing of cleaning/disinfection of environmental surfaces and patient-care equipment facilitates feedback as results are available within a minute and easily comprehensible. We provided standardized feedback on the study’s results to staff responsible for cleaning to reiterate the importance and effectiveness of their efforts. Feedback compared to cleaning alone did not enhance pass rates in the combined results for all surfaces although changes were seen for some surfaces, e.g., front desk, exam room table (Figure 2). Feedback has been shown to enhance cleaning effectiveness in the setting of terminal cleaning of hospital rooms. ^{Reference Branch-Elliman, Robillard and McCarthy20,Reference Martin, Salsgiver and Bernstein21} A recent multicenter randomized trial evaluated effectiveness of different methods of cleanliness monitoring compared to ultraviolet/ fluorescent marker detection and feedback, ATP monitoring and feedback was associated with a significant reduction in cleaning failures and in the incidence rate of multi-drug resistant organism (MDRO) infection and colonization in ICUs. ^{Reference Ziegler, Babcock and Welbel22}

Concerns about ATP technology exist. ^{Reference Whiteley, Derry and Glasbey23} Sciortino et al. compared different commercial ATP luminometers to assess repeatability, linear range, and reproducibility using defined, experimental bacterial inocula placed on stainless steel surfaces. ^{Reference Sciortino and Giles24} In their model, the instrument used in our study detected ATP for as long as 10 days and provided good linearity of results between 10² to 10⁷ CFU for three test organisms (S. aureus. Acinetobacter baumannii, and Candida albicans). However, the instrument showed higher inter-operator differences than other luminometers suggesting that training for the sampling method is important. ^{Reference Sciortino and Giles24} To facilitate training, we provided direct communication via audio-visual meetings, written instructions, and additionally an instructional video to all study personnel to standardize surface sampling. Surface testing was done by the same person at each clinic (except two testing rounds in one clinic)—and in the 9 centers that had pediatric and adult clinics, the same person sampled the surfaces which served to reduce inter-person variations. Several cleaning agents can lead to quenching of ATP. ^{Reference Omidbakhsh, Ahmadpour and Kenny25,Reference Moore, Smyth and Singleton26} , which can potentially lead to higher pass-rates. Thus, comparisons with baseline measures are recommended. Baseline pass-rates here were high compared to other publications that were done in inpatient settings or ICUs. ^{Reference Boyce, Havill and Dumigan2,Reference Moore, Smyth and Singleton26} Possible explanations are the short stay in outpatient clinics compared to inpatient care and sampling areas next to the patient in ICUs. Potentially high attention to cleaning by staff working in the clinics who are instructed to clean immediately after the patient contact also contribute. The variations of RLU within the same study site indicate that failures do occur and that ongoing education is helpful.

Studies have also shown that correlation between RLU values and CFU ranged from significant to very poor, which supports using set cut-off benchmarks rather than actual values. ^{Reference Nante, Ceriale and Messina3,Reference Lewis, Griffith and Gallo6} The lack of correlation may be explained by technical aspects; i.e.; other organic material (e.g., blood cells, sloughed skin cells) reacting with the assay reagents. As such, RLU to CFU comparisons were much better in studies using defined bacterial solutions rather than surfaces. ^{Reference Sciortino and Giles24} Several studies have evaluated different RLU cut-off values to consider a surface “clean” – ranging between 100 and 500 RLU. A recent metanalysis showed a cut-off of 250 RLU to be most common across studies, yet the cut-off should be based on the recommendations of the specific ATP system used. ^{Reference Nante, Ceriale and Messina3} We chose a value of < 250 RLU as the passing cut-off based on the manufacturer’s recommendations and our prior work, which showed this cut off had acceptable sensitivity and specificity when compared to CFU counts. ^{Reference Salsgiver, Bernstein and Simon4,Reference Mulvey, Redding and Robertson27}

Limitations of our study include lack of generalizability as participating sites were large CF care centers. Furthermore, our sample size was relatively small compared to the ∼110 accredited CF centers in the U.S. We selected frequently touched surfaces based on the investigators’ experience and prior observations of surfaces frequently touched by staff, e.g., computer keyboards and computer mouse. ^{Reference Huslage, Rutala and Sickbert-Bennett28,Reference Weinstein29} However we did not measure touching frequency at the study sites. Prior studies testing the impact of improved cleaning on infection rates were conducted for inpatients who have a longer exposure to the hospital environment than those in clinic. ^{Reference Ziegler, Babcock and Welbel22,Reference Moore, Smyth and Singleton26} Therefore, we cannot extrapolate our findings to reduced infections for outpatient clinics. The Hawthorne effect may have influenced results as staff had been informed about the study although staff did not know exactly when ATP testing would occur. Although this study was conducted after the height of the SARS-CoV-2 pandemic, there may have been increased attention to IP&C practices. However, study sites confirmed that patient volumes and clinic flow had returned to pre-pandemic levels. ^{Reference Muhlebach, Cunningham and LiPuma30} . Thus, we expected opportunities for contamination of environmental surfaces and patient care equipment to be similar to that experienced prior to the pandemic. Finally, we do not know the long-term effectiveness of the feedback or sustainability of this intervention.

In summary our study findings demonstrated the feasibility of using an ATP bioluminescence assay to measure cleanliness of environmental surfaces and patient care equipment in ambulatory settings caring for pwCF. Differences found between the cleanliness of pediatric versus adult clinics can inform centers about the challenges cleaning clinics that care for younger patients and the possible sources of transmissible pathogens. Further larger quality improvement efforts focusing on surface and equipment cleaning in CF care settings are desirable as is determining sustainability.