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infection control and hospital epidemiology Use of Gaseous Ozone for Eradication
mg/L), and linezolid (MIC, 0.75 mg/L), and was susceptibleto mupirocin by disk diffusion; the strain was resistant to of Methicillin-Resistant Staphylococcus
oxacillin (MIC, 24 mg/L) and erythromycin (MIC, 16 mg/L) aureus From the Home Environment
by E-test, and to clindamycin by disk diffusion test (disso- of a Colonized Hospital Employee
ciated resistance). The other patients on the ward and thepersonnel involved with her care were screened for MRSA.
Hero E. L. de Boer, MD;
In our institution, a set of screening cultures includes at least Carla M. van Elzelingen-Dekker, BSc;
nose, throat, and perineum swab specimens and, for persons Cora M. F. van Rheenen-Verberg, BSc;
with eczema or skin lesions, a skin swab specimen. Two other Lodewijk Spanjaard, MD, PhD
patients and 2 nurses carried the same strain of MRSA. After8 weeks, all colonized patients had been discharged and 1nurse had multiple cultures negative for MRSA.
An intensive care nurse with eczema was repeatedly treated for meth- Cultures of additional swab specimens of the nose and skin icillin-resistant Staphylococcus aureus (MRSA) carriage. Because cul- lesions from the other nurse remained positive for MRSA (Fig- tures remained positive for MRSA, her house was investigated.
ure). She had constitutional eczema with continually fluctu- Thirty-four percent of environmental samples yielded MRSA. Her ating activity, which was treated with several creams. MRSA children and cat were free of MRSA. The house was decontaminated eradication treatment was initiated (Figure). In our institution, with gaseous ozone. All subsequent cultures were negative for MRSA.
this approach is only attempted when eczema is quiescent. The This decontamination cost i2,000 (approximately $2,400).
initial culture after the initiation of MRSA eradication treat- Infect Control Hosp Epidemiol 2006; 27:1120-1122 ment was negative for MRSA, but later cultures revealed con-tinuing carriage. Three additional courses of anti-MRSA treat- In most countries, methicillin-resistant Staphylococcus aureus ment were prescribed. Antimicrobial agents used in the 5 (MRSA) is widespread in hospitals. In The Netherlands, na- courses of treatment (the duration of all treatments was 7 days) tional policy is to keep the prevalence of MRSA at the current were as follows: courses 1 and 3, mupirocin nasal ointment, level of less than 1% of all S. aureus isolates.1 Because hospital chlorhexidine scrub, and vancomycin (250 mg orally every 6 employees’ hands are an important route of transmission of hours); course 2, mupirocin nasal ointment, chlorhexidine MRSA, cultures are regularly collected from staff in contact scrub, vancomycin (250 mg orally every 6 hours), rifampin with an MRSA-colonized patient to identify carriage. Em- (600 mg orally every 24 hours), and doxycycline (100 mg orally ployees carrying MRSA are treated with a variety of measures, every 24 hours); and courses 4 and 5, mupirocin nasal oint- including administration of mupirocin nasal ointment, chlor- ment, chlorhexidine scrub, vancomycin (250 mg orally every hexidine scrub, and orally administered antimicrobial agents.
6 hours), doxycycline (100 mg orally every 24 hours), and Failure to eradicate carriage is often associated with a risk linezolid (600 mg orally every 12 hours).
factor (eg, eczema or wounds), but reinfection after successful Because the nurse had persistent MRSA colonization, re- eradication also occurs. A possible source of MRSA outside training for another post was considered. She became de- hospitals is the home environment, including family mem- pressed because of the threat of a switch from her favored bers, pets, and surfaces of furniture. We could not find a occupation and was treated with antidepressants. After the published report of disinfection of rooms and furniture with fourth course of anti-MRSA treatment, results of 3 weekly ozone, which is often used as an industrial disinfectant but culture sets were negative, and she returned to work in Oc- infrequently tested for possible medical applications.2-6 This tober 2002. However, screening cultures were positive for report describes the successful use of gaseous ozone to erad- MRSA a month later. All MRSA isolates from the nurse icate MRSA in the home environment, which was responsible showed the same susceptibility pattern, as did the isolates for repeated infection of a nurse with eczema who had re- from the index patient, the contact patients, and the other nurse. The possibility of reinfection in the home was con-sidered, and environmental screening of her house was per- formed 2 weeks later. Thirty-two sites in the house were In December 2001, cultures of specimens from a pediatric sampled using sweep plates containing mannitol salt agar with intensive care patient unexpectedly yielded MRSA (phage type 2 mg/L of oxacillin. In addition, swab specimens from her 2 I64). By E-test (AB Biodisk), the strain was susceptible to children (nose, throat, and perineum specimens) and her cat tetracycline (minimal inhibitory concentration [MIC], 0.094 (throat, perineum, and coat specimens) were obtained. Eleven mg/L), trimethoprim-sulfamethoxazole (MIC, 0.75 ϩ 14.25 (34%) of the environmental cultures yielded MRSA (Table).
mg/L), vancomycin (MIC, 1.5 mg/L), rifampin (MIC, !0.016 Her children and the cat tested negative for MRSA.
ozone for mrsa decontamination of the home Culture results for the nurse colonized with methicillin-resistant Staphylococcus aureus (MRSA) and control measures used, A salvage company was asked to decontaminate the house.
The company advised discarding the carpet, couch, and cur-tains and using gaseous ozone for all rooms of the house.
It is difficult to eradicate MRSA from a carrier with eczema, The rooms were treated one after the other. Metal objects especially when present on the hands. The risk of MRSA were temporarily put in another room. An ozone generator spreading into the environment is significant because of the and ventilators were placed in the house to circulate the high shedding of skin flakes. If eczema is in remission and ozone, which is heavier than air. The generator produced multiple courses of eradication therapy fail, the most likely approximately 35 g of ozone during 10 hours and was re- cause is reinfection from family members, pets, or the home moved after 24 hours. The concentration of ozone was es- environment. The last possibility appears most plausible in timated at 12 ppm but was not measured. Each room was this case, because the family members and pet were free of hermetically closed during the decontamination period and MRSA. This means that the staphylococci should have sur- was subsequently thoroughly ventilated. The nurse, her 2 chil- vived approximately 6 weeks in the home environment (Fig- dren, and the cat stayed with relatives for a week. Then the ure). Studies have shown that some MRSA isolates can in- nurse was treated again. Two days after the house was cleaned, deed survive in dust or on synthetics for more than 5 several specimens for culture were obtained from the house weeks.7,8 Environmental MRSA eradication should be care- and the nurse. All yielded negative results, and the nurse fully planned, and the choice of the method for disinfection started working again in April 2003. Swab specimens of the of rooms and furniture needs to be considered. Commonly nose, throat, perineum, and skin lesions were obtained used hospital disinfectants, such as ethanol, chlorine, and monthly until April 2004 and again in September 2005. All disinfectants that are less often used in The Netherlands, such cultures remained negative for MRSA. The cost of this de- as phenolics and quaternary ammonium compounds, are not contamination procedure was i2,000 (approximately $2,400: appropriate for use with house furniture.
salvage company, i1,500; discarded furniture, i500), which Two studies have described decontamination of the home environment for refractory MRSA carriage in healthcare table. Results of Cultures of Specimens Obtained From the Home EnvironmentBefore Ozone Disinfection Armchair, carpet, cat’s scratching post, curtains, piano, remote control, andtelephone MRSA, methicillin-resistant Staphylococcus aureus.
infection control and hospital epidemiology workers.9,10 Allen et al.9 used a general-purpose detergent to we describe the successful use of gaseous ozone to eradicate thoroughly clean all hard furnishings, whereas all carpets and MRSA from a widely contaminated home environment.
soft furnishings were steam-cleaned. Masterton et al.10 statedthat the house was thoroughly vacuumed and damp dusted.
In both situations, some of the old furniture was replaced, We thank the nurse and her family, for their cooperation; Mr. A. de Reus and the hospital employee was treated together with MRSA- and Mr. E. Meijer, for advice; Dr. R. Behrens, for critical review of the text; colonized family members. All remained free of MRSA.
and the National Institute of Public Health and the Environment (Bilthoven), Ozone is often used as a disinfectant in the pharmaceutical and food industry and as a disinfectant of water and con-taminated cloths. It is the treatment of choice to clean a houseafter a fire, to eliminate the foul burnt smell. Only a few From the Departments of Occupational Health (H.E.L.d.B) and Medical Microbiology (C.M.v.E.-D., C.M.F.v.R.-V., L.S.), Academic Medical Center, studies describe possible medical applications of ozone,2,3 be- cause it is toxic, necessitating respiratory protection for work- Address reprint requests to Lodewijk Spanjaard, MD, PhD, Laboratory of ers, and as a potent oxidizer is detrimental to metals. Ozone Bacteriology, Academic Medical Center, L-1-243, P.O. Box 22660, 1100 DD oxidizes the bacterial cell wall and cytoplasmic membrane, Amsterdam, The Netherlands (
and fungi are equally susceptible. The dose response for mi- Received March 18, 2005; accepted March 18, 2006; electronically pub- croorganism inactivation is in the following order (low to ᭧ 2006 by The Society for Healthcare Epidemiology of America. All rights high dose): gram-negative bacteria, vegetative gram-positive reserved. 0899-823X/2006/2710-0017$15.00.
bacteria, yeasts, molds, and Bacillus spores.5,6 The ozone con-centration necessary to kill MRSA appears to be higher than that needed to kill methicillin-sensitive S. aureus.2,4 Berring-ton and Pedler2 tested the effect of gaseous ozone on MRSA 1. Tiemersma EW, Bronzwaer SL, Lyytikainen O, et al. Methicillin-resistant in hospital rooms. They found that not all places in the room Staphylococcus aureus in Europe, 1999-2002. Emerg Infect Dis 2004; 10: became free of MRSA and therefore concluded that this 2. Berrington AW, Pedler SJ. Investigation of gaseous ozone for MRSA method was inadequate for decontamination. However, they decontamination of hospital side-rooms. J Hosp Infect 1998; 40:61-65.
ran the ozone generators for only 4-7 hours. On the basis of 3. Cardoso CC, Fiorini JE, Ferriera LR, Gurjao JW, Amaral LA. Disinfection the experience of the salvage company and the favorable result of hospital laundry using ozone: microbiological evaluation. Infect Con- in the present case, it appears wise to use generators for 10 trol Hosp Epidemiol 2000; 21:248.
hours, along with devices to circulate the ozone. The latter 4. Yamayoshi T, Tatsumi N. Microbicidal effects of ozone solution on meth- are necessary to disperse the gas equally, because gaseous icillin-resistant Staphylococcus aureus. Drugs Exp Clin Res 1993; 19:59-64.
5. Moore G, Griffith C, Peters A. Bactericidal properties of ozone and its ozone is heavier than air. All rooms should be tightly sealed potential application as a terminal disinfectant. J Food Prot 2000; 63: to prevent loss of ozone. After decontamination, specimens for screening cultures should be collected. During the de- 6. Li CS, Wang YC. Surface germicidal effects of ozone for microorganisms.
contamination period, all inhabitants need to be accom- AIHA (Fairfax, VA) 2003; 64:533-537.
modated elsewhere and MRSA carriers must be treated to 7. Neely AN, Maley MP. Survival of enterococci and staphylococci on hos- pital fabrics and plastic. J Clin Microbiol 2000; 38:724-726.
8. Wagenvoort JH, Penders RJ. Long-term in-vitro survival of an epidemic The cost of ozone cleaning and disinfection was i2,000 MRSA phage-group III-29 strain. J Hosp Infect 1997; 35:322-325.
(approximately $2,400). In 1997, Allen et al.9 reported the 9. Allen KD, Anson JJ, Parsons LA, Frost NG. Staff carriage of methicillin- cost for cleaning, laundering, and replacement of furnishings resistant Staphylococcus aureus (EMRSA 15) and the home environment: to be approximately £2,000 (approximately $3,500).
a case report. J Hosp Infect 1997; 35:307-311.
10. Masterton RG, Coia JE, Notman AW, Kempton-Smith L, Cookson BD.
In conclusion, we describe how environmental screening Refractory methicillin-resistant Staphylococcus aureus carriage associated is essential for investigating refractory MRSA carriage, even with contamination of the home environment. J Hosp Infect 1995; 29: in the presence of a risk factor such as eczema. Furthermore,



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