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Multidrug-resistant Candida auris infection has been reported from five continents in recent years. The prevalence of C. auris invasive infection has been estimated at 5.3% for intensive-care-acquired candidaemia in India. The transmission of the organism between the patients and from environment to patients is rapid.
To understand the intra-hospital dynamics of C. auris transmission and to determine the possible interventions to prevent its spread.
Surveillance of intensive care units was carried out to assess patient colonization, environmental contamination and hand carriage of the yeast among healthcare workers. Interventions including chlorhexidine washing of patients and decontamination of environmental surfaces with stabilized hydrogen peroxide disinfectant (Ecoshield) were undertaken. We further evaluated the effectiveness of frequently used disinfectants in the hospital against C. auris on various inanimate surfaces, and its persistence on hospital fabrics.
Three cases of C. auris bloodstream infection were detected over a period of three months. Many patients admitted at the same time, in the same area, were colonized by C. auris. Surveillance detected C. auris contamination of environmental surfaces and hands of healthcare workers. Interventions such as chlorhexidine washing and appropriate use of disinfectants could eradicate C. auris from patients and hospital environment.
The frequently used disinfectants in our hospital and current hand hygiene practices were efficient against C. auris if proper contact time and procedures were followed. Evaluation of possible persistence of C. auris on dry fabrics showed that they can persist for up to seven days.
]. However, the burden of the C. auris infection remains unknown, because the majority of the studies are from single centres without known denominators. A study covering 27 intensive care units (ICUs) in India in 2011–2012 reported C. auris as the fifth most frequent cause of candidaemia, accounting for 74 out of 1400 (5.3%) cases [
]. In a subset case–control analysis of the same study, longer duration of ICU stay, multiple invasive procedures, and previous antifungal therapies were identified as the major risk factors for C. auris infection [
In a study from the USA, whole genome sequence analysis of 54 isolates collected from multiple geographical locations differentiated isolates into four clades: South Asia, South Africa, South America, and East Asia. There were minor differences among the isolates within the same geographical region. The study suggested simultaneous emergence of C. auris infection at multiple geographical locations, rather than spread from one place to another [
]. Though it is generally believed that C. auris is acquired nosocomially, the source of C. auris in hospital remains unknown. However, independent introductions of multiple C. auris clonal lineages into the same hospital has been demonstrated, suggesting the possibility of community reservoirs [
]. However, in an outbreak investigation at a cardiac hospital in the UK, C. auris was isolated from the colonizing site in only one of 2246 (0.04%) patients screened at the time of admission, indicating the hospital as the likely source of the organism [
]. The ecological niche of this yeast within the hospital has been the subject of multiple investigations without any success, though the fungus has been isolated from multiple areas in the patient environment [
]. It is important to understand the intra-hospital dynamics of infected and colonized patients – this would help to implement control and eradication measures.
The Postgraduate Institute of Medical Education and Research (PGIMER) is a tertiary care multi-specialty hospital in northern India. Patients are referred directly from the community as well as from other hospitals. We therefore followed three cases of invasive Candida auris infection that occurred in our ICUs from January to March 2017 and attempted to identify the route of colonization, degree of environmental contamination by infected or colonized patients, as well as the effectiveness of control measures.
Patients were screened for C. auris colonization at four sites (axilla, groin, oral cavity, and rectal mucosa). Sterile cotton swabs (Himedia PW005, India) moistened with sterile normal saline (0.9%) were used to swab sites. Swabs were directly transported to the laboratory in a sterile tube, and inoculated on to Sabouraud dextrose agar (SDA). Plates were incubated at 37°C for 48h. Any growth detected was subjected to matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) identification.
Environmental samples were collected using sterile cotton swabs (Himedia PW005, Mumbai, India) moistened with sterile normal saline (0.9%). Swabs were then rolled on the surface of the inanimate objects or fomites in ICU. Swabs were directly transported to the laboratory in a sterile tube, and inoculated on to SDA. Plates were incubated at 37°C for 48h. Any growth detected was subjected to MALDI-TOF MS identification.
Collection of handwash samples from healthcare workers
Hands of healthcare workers were sampled following the method described by Strausbaugh et al. [
]. In any area where C. auris surveillance was performed, handwash samples were taken from all healthcare workers present. Briefly, healthcare workers were asked to rub both hands in a sterile bag with Sabouraud dextrose (SD) broth containing chloramphenicol and gentamicin (50mg/L). Handwashing bags were then incubated at 37°C for 48h. Subculture was performed on SDA and positive cultures identified by MALDI-TOF MS.
Identification of C. auris
Candida auris was identified by MALDI-TOF MS (Bruker, Bremen, Germany) with a score of >2.0 and confirmed by sequencing of ITS and D1/D2 regions of ribosomal DNA [
In-vitro studies were conducted to determine the survival and persistence of C. auris on the surface of hospital linen. Linen and blankets used in hospital were cut into small pieces of ∼3cm2, autoclaved, and placed in glass Petri plates. Each piece of the linen/blanket was inoculated with 100μL of 106cfu/mL of C. auris. The plates were kept at room temperature. Every day, one piece each of the blanket and linen were removed aseptically and placed into 10mL of SD broth. After 48h of incubation at 37°C, one loop full of the broth was subcultured on SDA plates.
Efficacy of hand hygiene on C. auris
To assess the efficacy of hand hygiene disinfectants against C. auris, volunteers were asked to wash hands with soap and water, 70% alcohol hand rubs or alcohol hand rubs with 0.5% chlorhexidine gluconate (CHG). Four groups of three volunteers in each group were formed. The first group served as control group. Ten microlitres of 106cfu/mL C. auris was inoculated on to finger tips of all volunteers of the four groups and allowed to dry for around 15min. The fingerprint impressions were taken on SDA plates from the volunteers of the control group. The second group washed their hands with soap and water following the six steps recommended by the World Health Organization (WHO) [
Healthcare Infection Control Practices Advisory Committee. Society for Healthcare Epidemiology of America. Association for Professionals in Infection Control. Infectious Diseases Society of America. Hand Hygiene Task Force Guideline for hand hygiene in health-care settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.
]. The third group used alcohol hand rub with 0.5% CHG, and the fourth used 70% alcohol only. Fingerprint impressions were then taken after handwash or antiseptic rub, on SDA plates.
Efficacy of hospital disinfectants in clearance of C. auris
The susceptibility of two environmental isolates of C. auris to five disinfectants [2% glutaraldehyde, 1% and 2% sodium hypochlorite, 10% Ecoshield (stabilized hydrogen peroxide 11% w/v with silver nitrate formulation), 2% DesNet (didecyldimethyl ammonium chloride, a quaternary ammonium compound), and 5% phenol] frequently used in our hospital was determined. One C. albicans ATCC24433 isolate was used for comparison of efficacy.
Four types of surface (stainless steel, ceramic, plastic, and glass) were used for this experiment. All surfaces were autoclaved before testing, and disinfectants were diluted to in-use concentrations. A suspension containing 106cfu/mL of organisms (C. auris and C. albicans) was prepared in normal saline (0.9%). A 100μL suspension each of the three isolates was spotted on to the different surfaces. After inoculation, surfaces were allowed to dry for a period of one hour, prior to adding disinfectants. After drying, 100μL of respective disinfectant was applied on to the spot. For the control, normal saline was used. The disinfectants were allowed to act for the recommended contact periods (Ecoshield, phenol and DesNet: 60min; glutaraldehyde: 20min; sodium hypochlorite: 10min). The inoculated surfaces were then swabbed.
Each swab was then vortexed in 1mL of neutralizing broth (Difco) and serial dilutions of 1:10, 1:100, and 1:1000 were prepared. SDA plates were inoculated according to Miles and Misra's method [
]. Each test was carried out in triplicate. Plates were then incubated at 37°C and assessed after 72h of incubation. The numbers of colonies were counted and multiplied by the dilution factor to calculate the total count of the organism. For all surfaces, the same technique was followed and was performed by a single person to avoid inter-individual variation.
MDR C. auris: C. auris with elevated minimum inhibitory concentrations to two or more classes of antifungal drugs was taken as multidrug resistant.
Candidaemia: The isolation of any Candida species from blood cultures. A case was defined as hospital-acquired C. auris candidaemia, if it occurred, 48h after hospital admission.
Colonization: Isolation of C. auris from any of the following body sites, including axilla, groin, oral cavity, or rectum of an asymptomatic patient.
Colonization clearance: If patients previously colonized with C. auris at any site (axilla, groin, oral and rectum samples) failed to grow the organism on subsequent sampling.
Hand carriage clearance: If C. auris could not be isolated from subsequent handwash samples of any healthcare worker who had previously been harbouring this yeast.
Follow-up of three cases of C. auris candidaemia
Case study 1
A female patient aged 57 years, with a history of atrial fibrillation and hypertension, presented to the emergency department on January 2nd, 2017, with chest pain and altered sensorium. She was transferred to the adult medical ICU (MICU), and after nine days moved to a female medical ward, and then finally to the cardiac care unit (CCU). As a routine procedure for CCU, blood cultures were performed on January 14th from both the central venous catheter (CVC) and the peripheral venous catheter, although the patient had no features of sepsis. Both the samples grew yeasts on automated blood culture (Bactec 9240, Becton Dickinson, MD, USA), which was identified as C. auris by MALDI-TOF MS and sequencing of ITS and D1/D2 regions of ribosomal DNA [
]. The CVC and peripheral lines were removed following laboratory report of C. auris isolation. As the patient was clinically stable without any signs and symptoms of sepsis, the treating physician did not start any antifungal agent and maintained a close watch on clinical parameters. A repeat blood sample was not collected after the removal of the catheter.
An investigation of the environment and healthcare workers' hands was conducted in the CCU to trace any possible sources. The patient's oral cavity, axilla, groin, forehead and neck were sampled after removal of lines, but C. auris was not isolated from any of these colonizing sites. The other patients admitted during the same period in the CCU were also screened for C. auris colonization (skin, oral and rectal mucosa), but the fungus was not isolated from any of these sites. A total of 81 environmental sites and 10 healthcare workers' hands were screened on CCU, but none of the samples yielded C. auris. Since the patient had spent nine days in the MICU on bed 7 (from January 2nd to 10th), we also screened MICU to look for a possible source (Figure 1). A total of 28 healthcare workers on the MICU were screened for carriage of C. auris in their hands. Each patient's oral mucosa, axilla, groin and rectum were also screened. Extensive environmental sampling was undertaken, including bed surfaces and handles of beds, blankets, medicine trolleys, ventilators, refrigerators, infusion pumps, suction bottles and tips, fluids (injectable medications, disinfectants in use), syringes, water, wash basins, taps, curtains, railings, door handles, glucometers, torch, stethoscopes, and mobile phones of doctors.
The sampling detected two patients in bed 1 and bed 6 of the MICU who were colonized with C. auris. C. auris was detected on the skin, oral and rectal mucosa of the patient in bed 1; and skin and oral mucosa of the patient in bed 6. The patient on bed 1 had already been admitted in MICU (date of admission December 29th, 2016) before the candidaemia patient. The patient in bed 6 had been admitted to MICU on January 6th until February 11th, 2017. C. auris was also found on the hand samples of one resident doctor and one nursing staff posted in MICU. Among the environmental surfaces sampled, special bed, bed 7, and the expiratory end of ventilator attached to bed 7 were positive for C. auris.
The next patient to occupy bed 7 in MICU (from January 11th to 20th) was discharged before the investigation period. Another patient arrived to occupy bed 7 on the evening of January 20th. This patient was sampled on January 22nd, but was not found to be colonized. Surveillance blood cultures were performed for all the MICU patients, but none cultured C. auris. The patient in bed 6 died due to disseminated tuberculosis on February 11th and the bed was occupied on the same day by another patient requiring ventilation. This patient was found to be colonized by C. auris on February 22nd, 11 days after occupying the bed. The patient in bed 1 was last screened on May 8th, and was negative.
Decontamination of the MICU environment was carried out with 5% phenol (carbolic acid) after C. auris had been detected from the environment. Repeat environmental samples on February 16th, four days post decontamination, were still positive for C. auris. A meeting of the infection control team with the MICU consultant doctors, nursing and paramedical staff was held to review the infection control protocols. This revealed that one bowl containing disinfectant was being used with a mop being repeatedly dipped into it. This meant that the phenol was unable to achieve adequate disinfection. Thus, a different disinfectant, Ecoshield (stabilized hydrogen peroxide 11% w/v with silver nitrate formulation) was recommended. A two-bowl method was implemented, using two separate stainless steel bowls, one containing water and other disinfectant. After cleaning, the mop was dipped in the water first, and then the disinfectant in the second bowl. The mop was allowed to remain in contact with the disinfectant for a prescribed period before being used again. Following this decontamination method, none of the environmental samples cultured C. auris. The cassette of the ventilator attached to bed 7 could not be adequately disinfected and it was replaced.
After a five-day gap, patients in MICU were screened again, and three of ten patients were found to be colonized (special bed, bed 1 and bed 6). To clean the body surface, washing with 2% CHG, and 0.5% chlorhexidine mouthwash were started for colonized patients on February 22nd. Post CHG decolonization, on March 3rd, two of the three patients were deemed clear of C. auris colonization. Repeat handwashing cultures (after 23 days) were also negative for the two healthcare workers from whose hands carriage of the yeast had been detected. Repeat screening conducted on May 8th showed that the third patient had also been cleared of C. auris colonization.
Case study 2
The second patient, a male aged 23 years, occupying bed 2 on the 12-bedded trauma ICU, was diagnosed on March 16th, 2017 with C. auris candidaemia (Figure 2). Enhanced surveillance (March 18th) was conducted in the trauma ICU following this event. Handwashings of healthcare workers, environmental sampling and screening samples from patients were collected. Only the axilla of the index patient (patient with C. auris candidaemia) and the infusion pump used on him detected C. auris. However, during a second round of surveillance (April 3rd), the surface of bed 2 and three newly admitted patients to the trauma ICU were found to be colonized with C. auris. The colonized patients had been admitted to bed 9 (oral, axilla, groin, and rectum colonized), bed 10 (oral, axilla, and rectum colonized) and bed 11 (axilla colonized). Due to our earlier experience at MICU, the disinfection protocol of trauma ICU was changed, and 10% Ecoshield was used to decontaminate the environment. The CHG washing was initiated for the colonized patients. Chlorhexidine mouthwash 0.5% was used by the patients, and oral colonization was cleared in patients in bed 9 and bed 10, but all three patients continued to remain colonized at other sites in successive screening.
In the third round of enhanced surveillance conducted on April 21st, the number of C. auris-colonized patients had increased to eight (patients on beds 1, 2, 3, 6, 7, 8, 10, and 11), and axilla colonization was noted in all patients. The environmental surveillance repeated on April 28th found that ECG leads (beds 1, 8, and 11) and blood pressure monitoring cuffs (bed 1) were contaminated with C. auris. With the suspicion that these materials remained close to axilla and might have led to a rise in number of axilla-colonized patients, 70% alcohol disinfection was recommended after each use. At the same time, from May 4th, ten consecutive patients newly admitted to trauma ICU were screened daily for determining the time of onset of colonization. The patients were found to be free of colonization on the day of admission to trauma ICU, but by the fourth day, all ten patients acquired the yeast at one or more sites (Figure 3). The axilla was found to be colonized in all these 10 patients.
To look for an explanation for axilla colonization, a repeat surveillance was carried out. Temperature probes as well as echocardiogram (ECG) leads were found to be contaminated. The disinfection of all these items was observed closely and was found to be suboptimal. It was noted that a bundle of leads was sprayed with 70% alcohol together and left to dry. The individual leads were not being meticulously disinfected with the alcohol. It was decided to decontaminate all these items with ethylene oxide sterilization.
From May 12th, the infection control team conducted intensive training of all staff working in the trauma ICU to emphasize strict infection control practices. The daily CHG washing was carried out under the direct supervision of the nursing chief of the ICU; and for heavily colonized patients (axilla and groin colonized) twice daily. Hand-hygiene practices were also observed. Two resident doctors from whom carriage of the yeast was detected were educated on performing adequate hand hygiene, based on the WHO-recommended ‘five moments’ and six steps of using soap or alcohol hand rub.
On May 28th, two patients (beds 2 and 11) remained colonized despite the CHG washing and ethylene oxide sterilization protocols. In these remaining two patients, a semiquantitative colony count showed a major reduction of count, from confluent growth to three to five colonies at the colonization sites. One patient was transferred to a high-dependency ward, where the CHG washing continued to be performed daily. This patient was finally discharged on May 30th, but the colonization status at discharge could not be checked. The other colonized patient in the trauma ICU remained colonized, despite twice-daily CHG washing in the oral cavity, groin, and rectum; although the growth of the yeast was scanty. Oral nystatin therapy was started for clearance but the patient died on June 14th due to cardiac arrest.
Case study 3
A male aged 66 years referred from another hospital was admitted in neurosurgery ward on March 14th, 2017. This patient was treated with an incomplete course of caspofungin (35mg/day) for a candida infection that had not been identified to a species level. A blood culture taken on March 15th grew C. auris and caspofungin (35mg per day) was restarted. The patient was transferred to MICU on March 19th. His rectum, axilla and groin were colonized with C. auris. This patient had a central venous line (CVC). Unfortunately, the CVC tip could not be cultured as the patient became agitated and removed the line. After 45 days of CHG washing and caspofungin therapy he became free of C. auris infection and colonization. The colonization and environmental surveillance of the neurosurgery ward performed on March 18th revealed that he was the only patient (of eight on the ward) colonized (axilla) with C. auris.
Surveillance and in-vitro experiments
Surveillance of hospital environment, patient colonization and HCW hand carriage
The environment, patients, and healthcare workers were sampled extensively during this study. A total of 7.9% (24/304) environmental samples, 21% (136/647) patient screening samples and 2.8% (4/145) of healthcare worker handwashings were positive for C. auris. Of all the body sites, the axilla was found to be the most frequently colonized site. Table I, Table II summarize the growth of C. auris from these samples.
Table IContamination of Candida auris on environmental samples and carriage on healthcare workers' hands
No. of samples
C. auris-positive samples
Handwash samples (HCWs)
No. of samples
C. auris-positive samples
MICU, medical intensive care unit; CCU, cardiac care unit; ICU, intensive care unit; NSW, neurosurgical ward; HCW, healthcare worker.
In-vitro experiments to determine persistence of C. auris on hospital linen
Candida auris persisted up to seven days on linen; no growth was detected on days 8, 9, and 10.
Efficacy of hand hygiene disinfectants on C. auris using volunteers
The fingerprint impressions of the control group showed confluent growth of C. auris. In the remaining three groups, there was no growth of C. auris after hand hygiene.
In-vitro experiment to determine susceptibility of C. auris to different disinfectants
There was no reduction of C. auris and C. albicans colony counts in the controls. All five disinfectants eradicated both C. albicans and C. auris on all surfaces tested when recommended contact time was allowed. For Ecoshield and 5% phenol (as they are routinely used for disinfection in our institute) efficacy was also checked for contact periods less than the recommended time. C. auris persisted if Ecoshield was removed before completion of adequate contact period (Figure 4). Susceptibility to CHG was also checked by this method and C. auris was found to be susceptible (100% log10 reduction) to 0.5%, 2%, and 4% concentrations at 2min.
The patients infected with C. auris had variable periods of stay in three ICUs (MICU, trauma ICU and CCU). Whereas the environment was contaminated with C. auris in MICU and trauma ICU, the yeast was not recovered from any patients, healthcare workers or environment in CCU. We were unable to explain the difference satisfactorily and there was no difference in disinfection policy among those areas. The blood culture of the index patient in CCU was positive, but we could not isolate C. auris from any of the colonizing sites of the patient, neither skin nor mucosa.
Prospective screening of patients admitted in trauma ICU revealed that none of the patients was colonized with C. auris at the time of admission to the hospital. However, they were rapidly colonized (within four days) during their stay in ICU. The observation indicates that C. auris is most likely acquired nosocomially. This confirms findings of the hospital in London where only one patient (0.04%) was found to be colonized among 2246 patients screened at admission to hospital [
]. They also showed that the patient once colonized remains colonized for months, which also occurred in two of our patients. Persistent colonization has also been reported in a study of seven patients infected in the USA [
]. In the present study, there was contamination of bed surfaces, and equipment such as ventilators, temperature probe and ECG leads. The contamination persisted for weeks around the bed surface, most probably due to the faulty disinfection practices in terms of inadequate contact time and concentration of phenol used at the beginning of the study. This persistent colonization of hospital environments and multiple body-sites of patients leads to high transmissibility and protracted outbreaks [
]. In an earlier study, there was a significant association with longer duration of central venous lines, urinary catheterization, postoperative drainage in patients, and relatively late acquisition of infection after ICU admission; which also supported the hypothesis of nosocomial transmission of C. auris in ICUs [
Though we could not identify the specific source of C. auris, it appeared to colonize the patient quickly after admission, and to contaminate the immediate vicinity of the patients as well as the hands of healthcare workers. Recently, Piedrahita et al. had reported that, like other yeasts, C. auris persisted better on moist areas compared to dry surfaces [
]. However, in our study the organism also persisted on dry linen and mattresses for up to seven days. We used three strategies: elimination from colonized sites using chlorhexidine body and mouth washes; elimination from the environment using disinfectants; and elimination from hands of healthcare workers by training and improvements in hand hygiene compliance.
Among the body sites screened, the axilla was the most frequent colonizing site. It is possible that contaminated ECG and other ventilator leads, as well as temperature probes, were the sources for high-frequency axilla colonization, due to their contact with the axilla in ventilated patients. Once these instruments had been disinfected properly, axillary colonization also decreased.
Despite twice-daily chlorhexidine body cleaning, two patients remained colonized in the groin, although the load of C. auris was substantially reduced. Both patients had diarrhoea and this possibly resulted in the persistent colonization of the groin in these patients. In this situation, these patients act as a potential reservoir of the pathogen in the ICU and can transmit the organism to other patients in case of breakdown in hand hygiene compliance or other infection prevention and control (IPC) measures. We were unable to get rid of gut colonization by C. auris. Nystatin has been used to clear C. auris from oral mucosa, and the same drug might be evaluated for gut eradication [
In the protracted London hospital outbreak of C. auris, stringent IPC measures such as strict isolation/cohorting and decolonization using chlorhexidine and oral nystatin were instituted. For terminal cleaning, fogging by hydrogen peroxide vapours was used to disinfect patient rooms [
]. Fogging was not attempted in our study as we did not have an alternative location for unstable patients in both ICUs. Being in the public sector, our hospital is usually over capacity. The situation would be similar in other public hospitals in India.
Candida auris was found to be susceptible to the most frequently used disinfectants in our hospital. In a recent study by Sherry et al., chlorhexidine was found to be effective at a concentration of 0.02% in eradicating both planktonic and sessile cells of C. auris [
]. The other disinfectants tested in our study have not been previously evaluated against C. auris. The relevance of testing these disinfectants is very high in developing countries due to frequency of usage.
Despite its susceptibility to frequently used disinfectants, C. auris initially persisted in the MICU after phenol disinfection. This could be due to inadequate contact time required due to the busy nature of the ICUs. When proper protocols (recommended concentration and contact time) were strictly adhered to, all contaminated surfaces were cleared of the yeast. Both Ecoshield and phenol were found to be effective using these protocols.
Similarly, hand hygiene performed according to the WHO-recommended steps effectively eradicated the yeast from finger tips. Hands of HCWs may be an important mode of transfer of this pathogen among patients and between different ICUs. We attempted to detect the possible source of C. auris in hospital water and food, but failed to isolate it (results not shown).
One limitation of the study is that we were unable to screen for rectal colonization in the majority of patients. We also did not screen healthcare workers for C. auris on body sites other than hands. Though we could not find the exact source of C. auris in the hospital, where the organism can potentially remain for long periods, patients appear to acquire it from the hospital environment and become rapidly colonized. Decolonization measures such as chlorhexidine washing seem to work in a majority of patients, but some patients may remain chronically colonized. The usual disinfectants and hand hygiene antiseptics are effective against C. auris, when recommended contact times for disinfectants and proper hand hygiene procedures are followed.
Conflict of interest statement
Candida auris sp. nov, a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital.
Healthcare Infection Control Practices Advisory Committee. Society for Healthcare Epidemiology of America. Association for Professionals in Infection Control. Infectious Diseases Society of America. Hand Hygiene Task Force
Guideline for hand hygiene in health-care settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.