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categorized according to the frequency of gram-negative organ- ism recovery by either method: 0–10%, 10%–20%, or >20%. A descriptive statistical analysis was conducted using SAS version 9.4 software (SAS Institute, Cary, NC). This study was acknowledged by the Johns Hopkins University institutional review board as nonhuman subjects research.
Results
In total, 229 HTSs were sampled in 17 unique patient rooms from May to December 2016. Of 17 patient rooms, 8 (47%) had gram- negative bacteria detected from at least 1 HTS by either method, 2 (12%) had CRE recovered, 2 (12%) had a non-CRE carbapenem- resistant organism recovered, and 7 (41%) had other or additional gram-negative organisms (Table 1). For the 2 rooms where CRE was detected, 1 was detected using the NFS method and 1 was detected using the CS method (Table 1, patients 3 and 5). Due to low overall recovery of CRE and non-CRE carbapenem-resistant organisms, we grouped these with all other gram-negative organism recovery to define the gold standard. The sensitivity for detection of any gram-negative organism in the environment was 100% for the NFS method and 21% for the CS method. Of the 8 positive rooms, 7 (88%) were identified using qualitative culture and 4 (50%) were identified by quantitative culture. The limit of detection for the NFS and CS methods was ~2×107 CFU/mL. Figure 1 shows the frequency of gram-negative organism recovery from HTSs in patient rooms and bathrooms.
Discussion
We infrequently recovered CRE in the rooms and bathrooms of inpatients known to be infected or colonized with CRE. Although we were unable to ascertain whether the NFS method or the CS
Clare Rock et al
method was superior at CRE recovery from environmental sur- faces, we did find some practical advantages of the NFS method. With the NFS method, the specific positive HTS is known, rather than the CS composite, where detected organisms could have been recovered from up to 5 HTSs. In addition, the NFS method requires less microbiologist time and expertise and less specialized equipment (ie, a stomacher or large centrifuge) than the CS method, making it less costly. Although, it took less time to process a single NFS (~8 mins) compared to a CS (~35 mins), the additional NFSs per patient room (up to 23) were more time intensive than the CS approach (up to 5 CS per room) due to the higher number of samples collected. Qualitative cultures had a higher sensitivity for gram-negative organism recovery than quantitative cultures. The NFS method is likely readily available in many healthcare facilities where they are used for patient multidrug-resistant organism (MDRO) surveillance programs, making it a feasible option when sampling the environment in a CRE outbreak situation or in research studies assessing cleaning practices. Some studies have favored different sampling methods over the NFS method for CRE recovery. An Israeli group com- pared recovery of Klebsiella pneumoniae carbapenemase and carbapenemase-producing Enterobacteriaceae in the hospital setting using contact plates and NFSs with either direct plating to Klebsiella pneumoniae carbapenemase selective agar or broth enrichment. They found enhanced recovery with contact plates: contact plate (32%) versus NFS with direct plating (24%) versus NFS with broth enrichment (16%).7 However, these researchers did not use neutralizer prior to sampling with NFS. The use of NFS with neutralizer rather than phosphate-buffered saline has been found to be superior at recovery of Staphylococcus aureus, and neutralizer used with the NFS method in this study may have helped with bacteria recovery.8 Another potential strength of our study design was accounting for the important confounding variable of right-hand dominance during cleaning, whereby we alternated which half of the HTS was sampled by each method. In this study, the environments of patients known to harbor
CRE were frequently contaminated with other gram-negative organisms. We are not aware of any other studies investigating all gram-negative organism recovery; however, gram-negative MDRO recovery can range from 1.8% to 30% of surfaces.9,10 Shams et al6 found 34% of HTSs to be contaminated with MDROs after daily cleaning, although these were mostly gram-positive MDROs. Our study has some limitations. The limit of detection for CRE
was ~2×107 CFU/mL. Therefore, it is possible that HTSs with a lower gram-negative organism burden may have given negative results using these sampling methods. Although we sampled a small number of patient rooms, this study supports the use of NFSs when recovering gram-negative organisms in the patient environment. The NFS method is more feasible due to decreased cost, increased availability, and less lab expertise necessary, and it may be advantageous during outbreak investigations because the specific contaminated HTS is identified.
Acknowledgments.
Financial support. This work was supported by funding from The Sherrilyn and Ken Fisher Center for Environmental Diseases and the National Institutes of Health (grant no. R21-AI130608) awarded to P.J.S., and from the Centers for Disease Control and Prevention (CDC) Epicenters Program to C.R., V.S., A.M.M., L.L.M., and P.J.S.
Fig. 1. Frequency of gram-negative organism recovery from high-touch surfaces in patient rooms and bathrooms.
Conflicts of interest. All authors report no conflicts of interest relevant to this article.
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