APPLIED MICROBIOLOGY, Feb. 1968, p. 223-227 Copyright 1968 American Society for Microbiology Vol. 16, No. 2 Printed in U.S.A. Terminal Disinfection in Hospitals with Quaternary Ammonium Compounds by Use of a Spray-Fog Technique HERMAN FRIEDMAN, ELAINE VOLIN, AND DAVID LAUMANN Department of Microbiology, Albert Einstein Medical Center, Philadelphia, Pennsylvania 19141 Received for publication 11 August 1967 Spray-fogging of hospital rooms with a quarternary ammonium disinfectant was found to be an effective means of reducing the number of detectable airborne and surface bacteria. The level of bacterial contamination in hospital rooms was determined before and after fogging by means of the gravitational fallout method, the petri dish swab technique, and volumetric air-sampling procedures. Rooms vacated by patients infected with staphylococci, streptococci, pseudomonads, and salmonellae were tested and found to be effectively decontaminated of most of the detectable organisms by the fogging procedure. Previous studies indicated that a spray-fog technique using a quarternary ammonium disinfectant is a useful adjunct for antimicrobial control of hospital rooms (1). Rooms in a general hospital were deliberately contaminated with aerosol suspensions of various strains of potentially infectious organisms, such as staphylococci, pseudomonads, and shigellae (1). Subsequent "fogging" with a quarternary disinfectant resulted in rapid removal of detectable airborne and surface contamination. The efficacy of such a fogging-disinfection procedure for removing a major portion of the detectable contaminating microbes in test hospital rooms suggested the use of this method as an adjunct for terminal disinfection of hospital areas. This investigation is concerned with the results of "field" trials in which this technique was used for disinfection in a large general hospital. Rooms in a special infectious disease unit, as well as rooms in several other areas where infected patients were quartered, were sprayfogged with quarternary ammonium disinfectants after the discharge of the infected patient and before the admission of a new patient. were closed, but not sealed, when the fogging technique was used. A high-velocity fogging apparatus (Bactol Micronizer, Parachlor Chemical Corp.) was filled with 1 quart (0.95 liter) of Bactol Micro-Mist (1). A direct spray, lasting 10 to 20 sec, was applied to all readily exposed surfaces, such as furniture, floors, and window sifls. The fogging apparatus was then placed in the center of the room, with the nozzle pointing upwards, and was turned on. Fogging was performed for 10 to 15 min, until all of the disinfectant was atomized. Immediately thereafter, the room was re-entered, the apparatus was turned off, windows were opened, and, if necessary, the air conditioner was turned on. General routine housekeeping procedures were then followed, including scrubbing of the floors, walls, and exposed portions of the furniture either with synthetic phenolics, or with a cleanser containing a phenolic and quarternary ammonium compound (Sani-Bactol, Parachlor Chemical Corp., New York, N.Y.). Detection of microbial contamination. Airborne and surface contamination in the rooms was determined by several means. (i) Gravitometric method: petri dishes, containing either blood-agar medium or Sabouraud agar, plus 1% Tween 80 for neutralization of disinfectant activity, were exposed in various areas of the room to obtain microbial "fallout" (1). The fallout rate per square foot was estimated as described previously (1), MATERIALS AND METHODS and the average number of fallout microbial particles Disinfectant. A commercially available quarternary per cubic foot of air was recorded. In addition, ammonium disinfectant (Bactol Micro-Mist, Parachlor Chemical Corp., New York, N.Y.), specifically Beef Extract and peptone, was used in several experi- Letheen broth, containing lecithin and Tween 80 in designed for spray-fogging, was used in this study. ments as the inoculum medium. The formulation of this disinfectant was previously (ii) Volumetric method: a volumetric air-sampling described in detail (1). apparatus, as described previously (1), was utilized Disinfecting procedures. Air conditioners, if in use for estimating bacterial contamination of air. All in test rooms, were turned off and doors and windows tests were done in duplicate with blood-agar and 223
224 FRIEDMAN, VOLIN, AND LAUMANN APPL. MICROBIOL. TABLE 1. Decrease in detectable airborne microorganisms before and after fogging of hospital rooms contaminated by patients infected with various pathogens No. of rooms with indicated per cent reduction Noofrooms Avg no. of Avg no. of of bacterial count Microbial pathogen No. of rooms mcrobes before microbes after - count or greater tetd fogging' fogginga 0-25% 26-50% 51-75% 76-100%/ or greater Staphylococcus 9 12.6 1.8 1 3 1 4 Streptococcus... 6 18.5 3.4 0 0 1 5 Salmonella... 7 11.3 2.6 1 0 3 3 Pseudomonas 5 19.1 4.5 0 1 2 2 Other... 6 15.1 3.1 1 0 2 3 Totals 33 15.3 3.1 3 4 12 14 a Bacteria per cubic foot. Sabouraud agar plates containing Tween 80. Microbial contamination was recorded as organisms per cubic foot. (iii) Surface cultures: microbial contamination of surfaces was determined by the "swab" technique using sterile cotton swabs (1). Direct colony counts were obtained by inoculating Brain Heart Infusion broth or Letheen broth with individual swabs, followed by transferring known quantities of the inoculum to agar pour plates. General procedure. The level of microbial contamination of individual hospital rooms was determined by the methods described above, at various times before and after the discharge of an infected patient. On the day of discharge, fallout plates and volumetric assays were performed within 1 hr prior to discharge. Following the discharge of a patient, the room was spray-fogged with 1 quart of quartemary ammonium disinfectant (Bactol Micro-Mist). After spray-fogging, surface cultures were obtained from various areas in the room, and the room was further disinfected by routine housekeeping procedure. Immediately thereafter and prior to admission of the next patient, volumetric air samples, as well as surface and fallout bacteriological counts, were obtained. A comparison was made between the microbial contamination of individual rooms disinfected by routine housekeeping technique plus fogging and those rooms which were cleaned but not fogged. RESULTS Fogging with quarternary ammonium disinfectant was found to be effective in decreasing the number of total detectable microorganisms in rooms vacated by infected patients. Table 1 presents the bacterial counts measured by a volumetric air-sampling technique prior to fogging as compared to results observed after fogging but before standard cleaning and disinfection procedures were carried out. There was a marked decrease in the number of recoverable pathogens in hospital rooms fogged with disinfectant after discharge of a patient. All rooms which had been FIG. 1. Comparison of the number of total detectable bacteria on surfaces offloors, walls, chairs, and tables prior to and immediately after fogging in rooms which had been occupied by patients with wound or systemic infections caused by several types of bacteria. occupied by patients infected with staphylococci, streptococci, salmonellae, or pseudomonads showed a marked reduction in recoverable bacteria after fogging (Table 1, Fig. 1). Although most rooms had an average of 10 to 15 detectable microorganisms per cubic foot of air sampled prior to fogging, there were usually less than two or three detectable microorganisms per cubic foot after fogging. Additional housekeeping sometimes further reduced the airborne bacterial counts. Results of bacterial swabbing and exposure of petri dishes (for detection of surface and airborne fallout of microbes) consistently indicated a marked reduction in the number of recoverable organisms after fogging (Fig. 1, 2). Swabs prepared from the surfaces of walls, chairs, or tables before and after fogging of rooms previously occupied by patients infected with a variety of
'VOL. 16, 1968 TERMINAL DISINFECTION IN HOSPITALS 225 prior to fogging. There was an average of 15 to 20 such recoverable bacteria per cm2 immediately following fogging, but before general routine housekeeping. In many instances, the recovered 4 E z FIG. 2. Comparison ofthe number of total detectable microorganisms per cm2 before and after fogging as determined by direct swab technique on floors of hospital rooms occupied by patients infected with staphylococci. Pre- and post-fogging swabs were obtained within I to 2 hr after patients' discharge. About one-third of detectable bacteria were Staphylococcus aureus. TABLE 2. Effect offogging on the number of detectable bacteria in hospital rooms as compared to routine housekeeping Bacteria Bacteria Treatment of roomsa No. of per ft*b per cm2c rooms Before After Before After Housekeeping only (no fogging)... 7 11.6 4.9 49.5 23.2 Fogging only (no housekeeping)... 9 13.8 2.1 34.7 3.8 Fogging followed by housekeeping. 17 18.3 2.2 50.5 1.3 Bacteriological determinations made immediately following the discharge of patient and immediately following final disinfection procedure. b Volumetric air counts. c Direct swab technique done on walls and floors of similar areas near patient's bed. infective bacteria, such as coagulase-positive staphylococci, streptococci, or salmonellae, invariably had fewer detectable microorganisms after disinfection. For example, data presented in Fig. 1 indicate that there were a total of 80 to 130 bacteria recovered per cm2 from simnilar areas on the floors, walls, and bedside tables of 27 rooms inhabited by infected patients immediately TABLE 3. Effect offogging on recovery of staphylococci in hospital room vacated by patient with staphylococcal wound infection Test After fogging Before fogging Before Af ter cleaning cleaninga Direct swabb Telephone 4+ 0 0 Chair 2+ 1+ 0 Bed 3+ 4 0 Floor 4+ 0 0 Wall 3+ 0 0 Petri plate exposurec 1 hr 2 0 0 2 hr 6 0 0 Volumetric counj9 Staphylococci 1.3 0 0 All bacteria 9.4 0.8 2.5 a Cleaning by general housekeeping method with phenolic-quarternary detergent (Sani-Bactol). b Comparative determination of staphylococci; 4+ = more than 100 colonies/cm2; 3+ = 70-100; 2+ = 30-70; 1+ = 5-30; 4 = 1-5. Number of staphylococci per petri plate, 15-min exposure. d Number of staphylococci and other bacteria per cubic foot. - 2i 0-0 -u 1. -o. u co E z, 15-0- * 6efore fogging after fogging Volumetric Air Sampling range Grovitometric Settling Method FIG. 3. Nwnber of detectable bacteria per cubic foot of air prior to and after fogging ofa hospital room occupied by a patient with a staphylococcal infection. Air sampling was performed by a volumetric air-sampling apparatus and a gravitometric fallout technique using open petri dishes.
226 FRIEDMAN, VOLIN, AND LAUMANN APPL. MICROBIOL. microorganism was identical to that associated with the infection. Figure 2 presents data pooled from several hospital rooms heavily contaminated with staphylococci from patients with pyogenic wound infections. There was a marked reduction in the number of detectable bacteria on solid surfaces within the rooms after fogging, but before general housekeeping, as compared to cultures immediately prior to fogging. Immediately after discharge of the patient, large numbers of staphylococci were isolated by the swab technique from the top of the bedside table, the seat of the bedside chairs, the floor in the patient's room near the bed, the bathroom floor, and the walls near the patient's bed. After spray-fogging, but before regular housekeeping procedures, there was a 90% or more reduction in number of recoverable staphylococci. In similar cases, where housekeeping procedures were performed but fogging was not, reduction in counts averaged about 50% (Table 2). Fogging plus housekeeping resulted in the most consistent reduction in the number of recoverable microorganisms. Quantitative determination of recoverable microorganisms by volumetric and petri plate exposure indicated that the most marked reduction occurred in rooms vacated by patients infected with staphylococci (Fig. 3). There was a severalfold reduction in the number of detectable organisms, both staphylococci and normal flora, when either the volumetric samples or exposed petri plates were used before and after fogging. Table 3 presents additional data from another room in which a patient was hospitalized owing to an infection caused by Staphylococcus aureus, coagulase-positive. Bacteriological data obtained before and immediately after disinfection by fogging indicated a significant decrease in the number of detectable microorganisms recovered by direct swab procedure and by volumetric testing for airborne bacteria. Additional routine housekeeping generally resulted in further decreases in the number of detectable bacteria. DIscUSSION Our results indicate that spray-fog disinfection with quarternary ammonium disinfectant is a useful adjunct for terminal disinfection of hospital rooms occupied by patients infected with pathogens, such as staphylococci, salmonellae, and similar microorganisms. Previous results indicated that spray-fog treatment of empty hospital rooms with quarternary ammonium compounds resulted in a marked reduction of airborne microorganisms, either normal flora or bacteria introduced by nebulization of a suspension of test organisms (1). The safety of fogging with toxic phenol disinfectants has been questioned (2, 3, 5). In the present study, it was observed that fogging with quarternary ammonium disinfectant did not result in any noticeable local or systemic irritation of housekeeping personnel, laboratory technicians, or new patients occupying the room within 1 hr after spray-fogging. Previous studies failed to reveal any pathological changes in mice exposed daily, for at least 6 weeks, to a disinfectant "fog" (1; H. Friedman and S. Sylk, unpublished data). Results of the present and previous studies demonstrate that fogging with a quarternary ammonium compound resulted in a marked decrease in the number of detectable bacteria over and above the decrease which was obtained by a general housekeeping procedure. However, the actual number of airborne microbes prior to disinfection was very low, generally less than 10 to 15 organisms per ft3 of air. Disinfection by fogging resulted in lowered counts. Most rooms occupied by infected patients contained pathogens in the air and on floor, walls, and furniture surfaces. Such pathogenic microorganisms were usually recovered readily by bacteriological sampling of various surfaces. Fewer organisms could be recovered from the same room after the spray-fog disintection, prior to cleaning (Fig. 1, 2, Table 1) or after cleaning (Fig. 3). On the other hand, when only general housekeeping disinfection was performed, even with phenol cleansers, many hospital rooms had more detectable pathogens than after fogging (H. Friedman and S. Sylk, unpublished data). There is no known accepted procedure for monitoring hospital areas or personnel for microbial contamination (3, 5-7, 9, 10). The three different techniques used in this study to determine bacterial contamination yielded the same results, suggesting that the decrease in detectable microorganisms after fogging is a valid finding and not the result of a redistribution of organisms from air to surfaces. Although there is no known method for demonstrating a causal relationship between the persistence of pathogens and infection of new patients or personnel, it is generally conceded by many hospital personnel that persistence of airborne organisms may be an important means of spreading infection throughout hospitals and among hospital staff (4, 6, 8-10). Thus, it is felt by some that a decrease in detectable pathogens in a hospital environment should be a major goal for disinfection procedures. Use of effective airdisinfection procedures is also thought to be of value in protecting housekeeping personnel, who are exposed to pathogens in an infected room prior to and during the housekeeping procedure. The results of the present investigation indicate
VOL. 16, 1968 TERMINAL DISINFECTrION IN HOSPITALS 227 that spray-fog disinfection with quarternary ammonium compounds is readily accepted by housekeeping personnel and is a valuable adjunct for reducing the number of detectable microorganisms in hospital rooms following the discharge of infected patients. AcKNowLmoGMENr The assistance of Howard Mann, Director of Housekeeping Services, Albert Einstein Medical Center, in the design and execution of this study is gratefully acknowledged. LITERATURE CLrr 1. FRIEDMAN, H., S. SYLK, AND D. LAUMANN. 1963. Evaluation of a spray-fog technique with quarternary ammonium disinfectant for antimicrobial control in hospital environments. Antimicrobial Agents and Chemotherapy- 1962, p. 66-75. 2. GRIFFTH, L. J. 1962. How effective are your disinfectants? Hosp. Mgmt. 94:45-48. 3. LUSKARIS, T. 1962. Methods of testing and comparing disinfectants. Hosp. Mgmt. 94:46-47. 4. OLDSTONE, M. B. A. 1966. Hospital-acquired staphylococcal infection. Role of air-borne organism. Am. Surgeon 32:391-398. 5. OSTRANDER, W. E., AND L. J. GRIFFITH. 1962. Selecting disinfectants for housekeeping use. Hosp. Mgmt. 94:48-49. 6. RILEY, R. L., Am F. O'GRADY. 1961. Airborne infection-transmission and control. The Mac- Millan Co., New York. 7. SPAULDING, E. H., ANm E. K. EMMONS. 1958. Chemical disinfections. Am. J. Nursing 58: 1238-1242. 8. WALTER, C. W. 1958. Environmental sepsis. Mod. Hosp. 91:69-78. 9. WILLIAMS, R. E. 0. 1960. Intramural spread of bacteria and virus in human populations. Ann. Rev. Microbiol. 14:43-64. 10. WILLIAMS, R. E. O., AND R. A. SHOOTER. 1963. Infection in hospitals. Epidemiology and control. F. A. Davis Co., Philadelphia.