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Impact of Detection, Education, Research and Decolonization without Isolation in Long-term care (DERAIL) on methicillin-resistant Staphylococcus aureus colonization and transmission at 3 long-term care facilities
American Journal of Infection Control 42 (2014) S269-S273
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Original article
Impact of Detection, Education, Research and Decolonization without Isolation in Long-term care (DERAIL) on methicillin-resistant Staphylococcus aureus colonization and transmission at 3 long-term care facilities Donna M. Schora MT(ASCP) a, *, Susan Boehm RN a, Sanchita Das MD a, Parul A. Patel MT(ASCP) a, Jennifer O’Brien MPH a, Carolyn Hines RN b, c, Deborah Burdsall RN d, Jennifer Beaumont MS e, Kari Peterson BA a, Maureen Fausone BA a, Lance R. Peterson MD a, f a
Department of Infectious Disease Research, NorthShore University HealthSystem, Evanston, IL Whitehall of Deerfield, Deerfield, IL Glenview Terrace, Glenview, IL d Lutheran Life Communities, Arlington Heights, IL e Department of Medical Social Sciences, Northwestern University, Evanston, IL f University of Chicago, Chicago, IL b c
Key Words: Long Term Care MRSA colonization Infection Prevention
We tested infection prevention strategies to limit exposure of long-term care facility residents to drugresistant pathogens in a prospective, cluster randomized 2-year trial involving 3 long-term care facilities (LTCFs) using methicillin-resistant Staphylococcus aureus (MRSA) as a model. We hypothesized that nasal MRSA surveillance using rapid quantitative polymerase chain reaction and decolonization of carriers would successfully lower overall MRSA colonization. In year 1, randomly assigned intervention units received decolonization with nasal mupirocin and chlorhexidine bathing and enhanced environmental cleaning with bleach every 4 months. Newly admitted MRSA nares-positive residents were decolonized on admission. Control units were screened but not decolonized. All units received periodic bleach environmental cleaning and instruction on hand hygiene. In year 2, all units followed intervention protocol caused by failure of the cluster randomized approach to sufficiently segregate patients. MRSA colonization was monitored using point prevalence testing every 4-6 months. Colonization status at admission and discharge was performed 1 quarter per year to determine acquisition. Fisher exact test was used for statistical analysis. Baseline MRSA colonization rate was 16.64%. In year 1, the colonization rate of intervention units was 11.61% (P ¼ .028) and 17.85% in control units (P ¼.613) compared with baseline. Intervention unit rate difference compared with the controls was significant (P ¼ .001). In year 2, the colonization rate was 10.55% (P < .001) compared with baseline. The transmission rates were 1.66% and 3.52% in years 1 and 2, respectively (P ¼ .034). The planned interventions of screening and decolonization were successful at lowering MRSA colonization. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Methicillin-resistant Staphylococcus aureus (MRSA) colonization rates in long-term care facilities (LTCF) can be high, with point prevalence surveys reporting rates of 7%-52%.1 Importantly, MRSA * Address correspondence to Donna M. Schora, MT(ASCP), NorthShore University HealthSystem, 2650 Ridge Ave, Walgreen Building, SB Rm #525, Evanston, IL 60201. E-mail address: [email protected] (D.M. Schora). This work was supported by the Agency for Healthcare Research and Quality (grant 1R18HS019968). Publication of this article was supported by the Agency for Healthcare Research and Quality (AHRQ). Conflicts of interest: None to report.
colonization is the key driver that leads to infection.2,3,4 Increased colonization puts LTCF residents at greater risk for infection.3,4 The cost of managing an LTCF resident patient with MRSA infection involves nursing care expense more than pharmaceutic or physician cost.5 The challenge for the LTCF staff is the mobility of the residents in a home-like atmosphere. Colonized residents are free to leave their room and congregate for meal times, activities on the unit, or within the facility. This mobility creates more chances for any organism to be spread by person to person contact and contamination of surfaces. Additionally, a room filled with personal
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.05.011
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Fig 1. Timeline of events for the 2-year study at 3 long-term care facilities. MRSA, methicillin-resistant Staphylococcus aureus.
items is harder to clean than an acute care patient room where these items are at a minimum. Measures to decrease the prevalence of dangerous nosocomial pathogens, particularly MRSA, in LTCFs are needed. We performed a research demonstration project in 3 LTCFs to create a model of acute care hospital and LTCF infection control collaboration by developing an LTCF-tailored intervention that reduced infection risk in older adults using MRSA as a proof of concept model. We hypothesized that one can safely remove the MRSA colonization risk from residents of the LTCF in a way that does not interfere with activities of daily living or socialization of residents. This was done by performing a federally registered, prospective, cluster randomized trial in the 3 LTCFs over 2 years (further study information is available from http://clinicaltrials.gov/ct2/ show/NCT01302210?term¼MRSAþinþLongþTermþCare&rank¼1). The strategy involved active surveillance using nasal swab samples, decolonization of carriers on intervention units, hand hygiene instruction, and enhanced cleaning of the environment. This strategy has been used successfully in another trial involving LTCF residents6 and with hospitalized patients in our own facility.2 We hypothesized that this strategy would be successful at lowering MRSA colonization and lead to less infection in this 3-facility LTCF trial. METHODS The study was performed in 12 nursing units at 3 LTCFs that are within 15 miles of each other. The 3 facilities have a combined total of 650-700 beds and 4,200 annual admissions. The units involved were from the following 3 categories: nursing, rehabilitation, and dementia care. The rehabilitation units were composed of mostly short-stay residents. The units at each LTCF were prospectively randomized by a statistician as intervention and nonintervention units. The study activities were carried out in the same manner at all 3 facilities and can be seen in the timeline in Figure 1. Two study nurses coordinated the events at all 3 sites and acted as liaisons with the onsite infection preventionist (IP) and medical director. To determine the burden of MRSA in each facility, 6 point prevalence surveys were conducted to determine if the prevalence of MRSA changed over time. To determine rates of acquisition, 2 periods of admission and discharge testing occurred, and those residents who were polymerase chain reaction (PCR) negative for MRSA on admission and PCR positive, culture positive at discharge were considered to have acquired MRSA. The program began in March 2011 with a point prevalence survey for MRSA nasal colonization at each facility to determine the prevalence of MRSA and identify those already colonized. A team of
study personnel collected a nasal sample from each resident over the course of 1-2 days at each LTCF. After the point prevalence, all residents on the intervention units were given a decolonization regimen of intranasal mupirocin ointment twice a day for 5 days and 1 chlorhexidine bath on the next scheduled bathing day (LTCF standard in Illinois is 1 bath per week). This decolonization regimen was repeated a second time 1 month later (based on preliminary study demonstrating this second decolonization was useful; data not shown). At the same time, in the intervention units, common areas, nursing units, equipment, and patient rooms were thoroughly cleaned with bleach. Hand hygiene education was given to all health care personnel at each LTCF. All admissions subsequent to the point prevalence had a nasal sample collected and tested on site for MRSA colonization within 24 hours. Samples were collected with a double-headed swab in Amies transport solution (Copan, Murrieta, CA). Residents with MRSA-positive nasal screen tests on the intervention units were reported to the nursing staff who then initiated decolonization with the mupirocin-chlorhexidine regimen. Positive patients on the nonintervention units were tested, but results were not reported to the staff, and no further action was taken. Contact isolation precautions were not initiated for any colonized residents in the intervention and nonintervention units at any time during the study. However, it was the policy at each LTCF to place MRSAinfected residents under contact precautions when identified by the infection preventionist as part of routine infection control practice. Point prevalence surveys were performed at 4-month intervals during the first year, along with environmental cleaning of all surfaces. At the end of year 1, for a period of 4 months, residents were screened for nasal MRSA colonization on admission and discharge. The admission and discharge samples provided a paired set of specimens, and the results from these samples were used to determine transmission. Residents that were leaving for home or another institution were sampled on the day of discharge. At the end of year 1, it was realized that during each day all intervention and control residents comingled with each other; therefore, all units were converted to the intervention protocol where all patients received decolonization when the MRSA test was positive. One LTCF continued with mupirocin decolonization; however, 2 others replaced mupirocin with retapamulin because of increasing mupirocin resistance in the MRSA isolates of the residents at these 2 LTCFs. Residents who failed 2 rounds of retapamulin decolonization were offered decolonization with oral rifampin and minocycline,6 with their written consent and the consent of their physician. Discharge testing was once again performed from January to March
D.M. Schora et al. / American Journal of Infection Control 42 (2014) S269-S273
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Table 1 MRSA colonization rates from point prevalence data Baseline
Year 1
Year 2
Nasal Screen Tests with MRSA PCR
Intervention
Control
Intervention
Control
Intervention
Control
Number of tests Positive MRSA tests* Culture prevalence (%)
315 53 16.83
358 59 16.48
715 83 11.61
762 136 17.85
1,044 134 12.84
1,230 106 8.62
*Confirmed by culture.
2013, and 2 additional point prevalence surveys occurred at the sixth and twelfth months of year 2. Infection control practices The infection prevention and control program at each LTCF was based on the regulatory requirements for long-term care.7 Prior to the study, infection prevention and control activities included daily informal surveillance and formal weekly infection prevention walking round observation (surveillance). Surveillance information was provided from a 24-hour report that included any resident condition change, culture results, new medications, transfers within the facility, and transfers to and from other health care facilities and the community. Information from formal and informal surveillance was combined with the culture results and antimicrobial prescriptions. The data were compiled and compared with the McGeer et al criteria for documenting an infection in the LTCF.8 A monthly report was completed that included infection rates, outbreak analysis, and quality improvement project results. Contact isolation was initiated when residents had signs and symptoms of an infection caused by a multidrug-resistant organism, Clostridium difficile infection, presence of draining and infected wounds pending culture results, unexplained rashes, nausea, vomiting, diarrhea without another noninfectious explanation, and signs and symptoms of a respiratory illness. Resident and patient rooms and common areas were cleaned daily with a quaternary product. Terminal room cleaning included use of bleach and detergent wipes on all high-touch areas, including toilets and sinks. Bleach and detergent cleaning were used in transmissionbased precautions rooms and all rooms during outbreaks. Statistical analytical methods Differences between time periods were evaluated using the Fisher exact test for proportions. PCR testing The nasal screen test was performed on site at each of the LTCFs with the Xpert MRSA PCR nasal test kit (Cepheid, Sunnyvale, CA). An instrument was placed at each LTCF so samples could be run 24 hours a day, 7 days a week. Either a study nurse or the resident’s nurse was notified that the sample was positive and decolonization could begin. Study personnel retrieved the positive samples and performed a culture on the remnant swab. The remnant swab was plated to a ChromAgar MRSA plate (BD Diagnostic Systems, Sparks, MD), and mauve colonies were subcultured to blood agar for further testing. Colonies resembling S aureus were tested with Staphaurex (Remel, Lenexa, KS) to confirm the identity of MRSA and then tested with an in-house developed PCR assay for the detection of high-level mupirocin resistance.9 The isolates also underwent typing analysis by pulsed-field gel electrophoresis to determine those isolates that were related or identical to each other. Pulsed field gel electrophoresis analysis of MRSA isolates The MRSA isolates were inoculated onto Columbia CNA agar (BD Diagnostic Systems, Sparks, MD) and incubated for 16-24 hours at 37 C. Pulsed-field gel electrophoresis was performed using the
restriction enzyme SmaI, as described previously,10,11 using S aureus NCTC 8325 as a control. Gel images were captured and digitalized as tagged image file format files using a Gel Doc XRþ system with Image Lab Software version 3.0 (Bio-Rad, Hercules, CA), and band comparisons were performed using BioNumerics software version 6.5 (Applied Maths Inc, Austin, TX). Dendrograms were generated for each comparison group using the unweighted pair group method based on arithmetic averages using Dice coefficients. Band tolerance and optimization were set at 1.25% and 0.8%, respectively. Pulsed-field band patterns were considered to be within the same cluster if they had a similarity coefficient 80% and identical if the similarity coefficient was 95%.11,12 This study was approved by the Institutional Review Board at NorthShore University HealthSystem (Protocol EH10-198). RESULTS MRSA nasal colonization rates were determined from the point prevalence surveys and are provided in Table 1. During the baseline period, the colonization rate in tested cultures was 16.64%. During year 1 of the study, the colonization rate was reduced to 11.61% in the intervention units (P ¼ .028) but remained stable at 17.85% in the control units (P ¼ .613) compared with baseline. The difference in rate between the intervention and control units was statistically significant (P ¼ .001). During year 2, when all units received the intervention, the colonization rate was 10.55%. The difference between baseline and year 2 was statistically significant (P < .001). Conversion rates were based on paired admission and discharge testing samples where the admission screen test was negative and the discharge screen was a PCR-positive, culture-positive test (Table 2). From year 1 to year 2, a significant increase in the transmission rate was observed, along with a smaller, nonsignificant increase in the admission prevalence. This change is driven primarily by the large and statistically significant changes in LTCF 1. Admission prevalence remained stable at LTCFs 2 and 3. Most conversions occurred on short-term stay units. For LTCF 1, 7 of 12 conversions were on short-term units. The average length of stay (LOS) for short-term unit conversions was 28 days; for long-term unit conversions it was 32 days. For LTCFs 2 and 3, 92% and 93% of conversions were on short-term units, respectively. The average LOS for a conversion on a short-term unit at LTCF 2 was 17.5; for LTCF 3 it was 28 days. The only long-term stay conversion at LTCF 2 was at 152 days; for LTCF 3, the conversion was at 42 days. The average LOS for short-term and long-term units at each facility during the course of the study can be found in Table 3. MRSA nasal isolates were available for molecular typing in 36 of the 39 residents who acquired MRSA as a result of transmission. In 22 of the 36 isolates, there was an identifiable, potential source of MRSA as evidenced by geographic proximity of the recipient isolate to a closely related or identical isolate. In 1 LTCF, identifiable isolates identical to those acquired could be traced to residents housed in rooms next to each other. Additionally, the results of PCR testing for mupirocin resistance can be found in Table 4.
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Table 2 Acquisition rates according to discharge testing during 1 quarter per study year Facility Total Number of residents sampled on admission Positive cultures on admission Admission prevalence (%) Number of residents sampled on discharge Culture negative on admission and positive at discharge Acquisition rate (%) LTCF 1 Number of residents sampled on admission Positive cultures on admission Admission prevalence (%) Number of residents sampled on discharge Culture negative on admission and positive at discharge Acquisition rate (%) LTCF 2 Number of residents sampled on admission Positive cultures on admission Admission prevalence (%) Number of residents sampled on discharge Culture negative on admission and positive at discharge Acquisition rate (%) LTCF 3 Number of residents sampled on admission Positive cultures on admission Admission prevalence (%) Number of residents sampled on discharge Culture negative on admission and positive at discharge Acquisition rate (%)
Year 1
Year 2
P value
1,708 58 3.40 725 12
1,206 50 4.15 767 27
.32
1.66
3.52
.034
543 7 1.29 205 1
395 15 3.80 271 11
.015
0.49
4.06
.016
720 16 2.22 324 6
509 13 2.55 304 9
.707
1.85
2.96
.438
445 35 7.87 196 5
302 22 7.28 192 7
.888
2.55
3.65
.572
Table 4 Mupirocin resistance rates in MRSA isolates found on admission to the 3 long-term care facilities Facility
Table 3 Average length of stay for long-term and short-term stay units at each long-term care facility Facility
Short-term stay unit
Long-term stay unit
LTCF 1 LTCF 2 LTCF 3
25 days 17.5 days 26 days
187 days 306 days 13 years
DISCUSSION In 2005, our health care system instituted universal admission screening for nasal colonization with MRSA.2 At that time we discovered that a large number of MRSA colonized patients entering our hospitals were from local LTCFs. Surgical patients are sent to rehabilitate in these LTCFs, making us part of the same health care team. Collaboration with the LTCFs on the reduction of MRSA colonization seemed like a natural next step. We reached out to LTCFs in the area and found willing partners. One LTCF outside of our health care system also requested participation. We began a demonstration project to create a model of hospital to LTCF infection control collaboration using the prevention of MRSA as a proof of concept model. Our goal was to develop LTCF-tailored interventions that reduced colonization and infection risk in older adults. An aim of the project was to show that one can safely remove the MRSA colonization risk from the residents in a way that does not affect their home-like style of living. The strategy involved some techniques that are typical in a hospital infection control program (eg, nasal surveillance testing, decolonization strategies, hand hygiene education, enhanced environmental cleaning regimens) but avoided other practices (eg, contact isolation practices for MRSA colonization). Nasal surveillance testing was performed on site at each LTCF by either a nurse or the study personnel using
LTCF 1 (%) LTCF 2 (%) LTCF 3 (%)
Year 1
Year 2
15.4 14.8 2.5
2.4 15.1 2.8
the Xpert MRSA PCR test. This assay is simple to perform, needs minimal supplies, has a small instrument footprint, and results are available within 1 hour. In this research project, nurses performed routine quality control and patient testing for the 2-year study without incident, and testing was easily implemented at the LTCF. Our results indicate that there was no difference in the MRSA prevalence rates when comparing intervention and control units at baseline, but statistical significance was seen in the intervention unit compared with baseline and from years 1 and 2 (Table 1). Because no other changes were implemented at the LTCF, the improvement was likely the result of the intervention. LOS of the residents at the time of acquisition had no effect because most conversions were on short-term stay units and their LOS was similar with the average at each LTCF. The MRSA acquisition increased somewhat from year 1 to year 2, and this increase was statistically significant (Table 2). It is unexplained and important that the increase did not impact the overall MRSA prevalence. In a recent report by Jones et al4 studying 1.4 million patient admissions in 112 hospitals in the Veterans Administration health care system, the authors found that a patient colonized or infected on admission imports MRSA into the hospital, and this admission prevalence contributes to the transmission risk. This investigation demonstrated that a 10% increase in a hospital’s average admission prevalence was associated with a 9.7% increase in the weekly acquisition rate.4 We did see an MRSA admission prevalence increase at LTCF 1 during discharge testing in year 2, and it was associated with a significant increase in transmission at LTCF 1, but this was not seen at the other facilities. This LTCF was the sole driver for the increase in the total acquisition rate. Although we have no explanation for the increase in MRSA-positive admissions at LTCF 1, it may explain an increase in acquisition rates and correlates with what was seen in the Veterans Administration report.4 Of interest was the need for the use of retapamulin for decolonization in year 2, which is understandable because 2 of the LTCFs (LTCFs 1 and 2) send their sick residents to hospitals that are within our health care system (and the third does not); during the period of this study, NorthShore was routinely decolonizing MRSApositive inpatients with mupirocin that had led to a mupirocin resistance rate in MRSA exceeding 10%. Therefore, LTCFs 1 and 2 likely had a higher rate of mupirocin resistance in their MRSA admission isolates in year 1 (Table 3) because of the rising resistance in our health care system.13 Therefore, in the second year of the study, residents of LTCFs 1 and 2 received retapamulin as a decolonization agent in place of mupirocin to maximize the success of the decolonization regimen. Critical to our research program, active surveillance, decolonization, and cleaning regimens did not appear to interrupt activities of daily living for the residents of the 3 LTCFs. There were no complaints by any residents, family, or staff about any components of this 2-year study. There are a few limitations to this research. Discharge testing was limited to 25% of the study period and involved mostly shortterm stay residents. If we had included residents who were negative at 1 point prevalence and positive at the next, it might have given us a broader picture of transmission at these LTCFs, but these activities did not capture all the residents staying in the LTCFs for the entire year; therefore, no accurate statistical assessment could
D.M. Schora et al. / American Journal of Infection Control 42 (2014) S269-S273
be made. Another potential limitation involved results from a project evaluating surveillance of MRSA colonization from 5 different body sites.14 Sites that were sampled included the nose, axilla, throat, perineum, and perianal areas. Only 81% of the residents sampled that were colonized with MRSA somewhere on their body were also colonized in their nose. Although we believe that nasal surveillance was sufficient for determining the prevalence of MRSA at the LTCF, it is possible that residents colonized at other sites may significantly contribute to MRSA spread and would not have been captured. Finally, not measuring LOS as a risk factor for MRSA acquisition is another potential limitation. However, this is a well-known risk factor and we were not studying risks for MRSA acquisition but rather whether colonization prevalence could be reduced. Studying LOS as a risk factor would require another research approach (eg, weekly nasal screening), something beyond the scope of this investigation. CONCLUSION The planned interventions of screening and decolonization were successful at lowering MRSA colonization in LTCF residents. A rise in MRSA transmission did not reverse this trend. The study interventions did not interrupt activities of daily living for the residents and could be implemented in other LTCFs. In-house (LTCF) PCR for MRSA was easily accomplished by nursing personnel and could be part of a comprehensive LTCF MRSA decolonization program, with testing done either before admission or at the time of entry into an LTCF. This collaboration between acute and long-term care resulted in an ongoing relationship between the acute care system and LTCF involved in the project. References 1. Reynolds C, Quan V, Kim D, Peterson E, Dunn J, Whealon M, et al. Methicillinresistant Staphylococcus aureus (MRSA) in 10 nursing homes in Orange County, California. Infect Control Hosp Epidemiol 2011;32:91-3.
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2. Robicsek A, Beaumont JL, Paule SM, Hacek DM, Thomson RB Jr, Kaul KL, et al. Universal surveillance for methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals. Ann Intern Med 2008;148:409-18. 3. Ridgway J, Peterson L, Brown E, Du H, Hebert C, Thomson R, et al. Clinical significance of methicillin-resistant Staphylococcus aureus colonization on hospital admission: one-year infection risk. PLoS One 2013;8:e79716. 4. Jones M, Ying J, Huttner B, Evans M, Maw M, Nielson C, et al. Relationships between the importation, transmission and nosocomial infections of methicillin-resistant Staphylococcus aureus: an observational study of 112 Veterans Affairs medical centers. Clin Infect Dis 2014;58:32-9. 5. Capitano B, Lesham OA, Nightingale CH, Nicolau DP. Cost effect of managing of methicillin-resistant Staphylococcus aureus in a long-term care facility. J Am Geriatr Soc 2003;51:10-6. 6. Bowler WA, Bresnahan J, Bradfish A, Fernandez C. An integrated approach to methicillin-resistant Staphylococcus aureus control in a rural, regional-referral healthcare setting. Infect Control Hosp Epidemiol 2010;31:269-75. 7. Department of Health & Human Services; Centers for Medicare and Medicaid Services (CMS) Tag F441. CMS manual system Pub. 100-07 state operations provider certification. Available from: https://www.cms.gov/Regulations-andGuidance/Guidance/Transmittals/downloads/r51soma.pdf. Accessed July 20, 2009. 8. McGeer A, Campbell B, Emori T, Hierholzer W, Jackson M, Nicolle L, et al. Definitions of infection for surveillance in long-term care facilities. Am J Infect Control 1991;19:1-7. 9. Hacek DM, Robb WJ, Paule SM, Kudrna JC, Stamos VP, Peterson LR. Staphylococcus aureus nasal decolonization in joint replacement surgery reduces infection. Clin Orthop Relat Res 2008;466:1349-55. 10. Jaggi P, Paule SM, Peterson LR, Tan TQ. Characteristics of Staphylococcus aureus infections, Chicago Pediatric Hospital. Emerg Infect Dis 2007;13: 311-4. 11. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, Tenover FC. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 2003;41:5113-20. 12. Limbago B, Fosheim GE, Schoonover V, Crane CE, Nadle J, Petit S, et al. Characterization of methicillin-resistant Staphylococcus aureus isolates collected in 2005 and 2006 from patients with invasive disease: a population-based analysis. J Clin Microbiol 2009;47:1344-51. 13. Dusich IK, Schora D, Peterson LR, Thomson RB Jr. Analysis of mupirocin susceptibility in a hospital setting utilizing mupirocin for decolonization of patients with nasal carriage of MRSA or MSSA. Proceedings of the 113th General Meeting of the American Society for Microbiology, 2013 May, 18-21, Denver, CO. 14. Schora DM, Boehm S, Das S, Patel PA, Schora K, Peterson KE, et al. Detection of methicillin-resistant Staphylococcus aureus (MRSA) from multiple body sites of residents at long-term care facilities. Advances in the Prevention and Control of Healthcare-Associated Infections. Available at: http://www.ahrq. gov/professionals/quality-patient-safety/patient-safety-resources/resources/ advances-in-hai/index.html. Accessed August 14, 2014.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Original article
Impact of Detection, Education, Research and Decolonization without Isolation in Long-term care (DERAIL) on methicillin-resistant Staphylococcus aureus colonization and transmission at 3 long-term care facilities Donna M. Schora MT(ASCP) a, *, Susan Boehm RN a, Sanchita Das MD a, Parul A. Patel MT(ASCP) a, Jennifer O’Brien MPH a, Carolyn Hines RN b, c, Deborah Burdsall RN d, Jennifer Beaumont MS e, Kari Peterson BA a, Maureen Fausone BA a, Lance R. Peterson MD a, f a
Department of Infectious Disease Research, NorthShore University HealthSystem, Evanston, IL Whitehall of Deerfield, Deerfield, IL Glenview Terrace, Glenview, IL d Lutheran Life Communities, Arlington Heights, IL e Department of Medical Social Sciences, Northwestern University, Evanston, IL f University of Chicago, Chicago, IL b c
Key Words: Long Term Care MRSA colonization Infection Prevention
We tested infection prevention strategies to limit exposure of long-term care facility residents to drugresistant pathogens in a prospective, cluster randomized 2-year trial involving 3 long-term care facilities (LTCFs) using methicillin-resistant Staphylococcus aureus (MRSA) as a model. We hypothesized that nasal MRSA surveillance using rapid quantitative polymerase chain reaction and decolonization of carriers would successfully lower overall MRSA colonization. In year 1, randomly assigned intervention units received decolonization with nasal mupirocin and chlorhexidine bathing and enhanced environmental cleaning with bleach every 4 months. Newly admitted MRSA nares-positive residents were decolonized on admission. Control units were screened but not decolonized. All units received periodic bleach environmental cleaning and instruction on hand hygiene. In year 2, all units followed intervention protocol caused by failure of the cluster randomized approach to sufficiently segregate patients. MRSA colonization was monitored using point prevalence testing every 4-6 months. Colonization status at admission and discharge was performed 1 quarter per year to determine acquisition. Fisher exact test was used for statistical analysis. Baseline MRSA colonization rate was 16.64%. In year 1, the colonization rate of intervention units was 11.61% (P ¼ .028) and 17.85% in control units (P ¼.613) compared with baseline. Intervention unit rate difference compared with the controls was significant (P ¼ .001). In year 2, the colonization rate was 10.55% (P < .001) compared with baseline. The transmission rates were 1.66% and 3.52% in years 1 and 2, respectively (P ¼ .034). The planned interventions of screening and decolonization were successful at lowering MRSA colonization. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Methicillin-resistant Staphylococcus aureus (MRSA) colonization rates in long-term care facilities (LTCF) can be high, with point prevalence surveys reporting rates of 7%-52%.1 Importantly, MRSA * Address correspondence to Donna M. Schora, MT(ASCP), NorthShore University HealthSystem, 2650 Ridge Ave, Walgreen Building, SB Rm #525, Evanston, IL 60201. E-mail address: [email protected] (D.M. Schora). This work was supported by the Agency for Healthcare Research and Quality (grant 1R18HS019968). Publication of this article was supported by the Agency for Healthcare Research and Quality (AHRQ). Conflicts of interest: None to report.
colonization is the key driver that leads to infection.2,3,4 Increased colonization puts LTCF residents at greater risk for infection.3,4 The cost of managing an LTCF resident patient with MRSA infection involves nursing care expense more than pharmaceutic or physician cost.5 The challenge for the LTCF staff is the mobility of the residents in a home-like atmosphere. Colonized residents are free to leave their room and congregate for meal times, activities on the unit, or within the facility. This mobility creates more chances for any organism to be spread by person to person contact and contamination of surfaces. Additionally, a room filled with personal
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.05.011
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Fig 1. Timeline of events for the 2-year study at 3 long-term care facilities. MRSA, methicillin-resistant Staphylococcus aureus.
items is harder to clean than an acute care patient room where these items are at a minimum. Measures to decrease the prevalence of dangerous nosocomial pathogens, particularly MRSA, in LTCFs are needed. We performed a research demonstration project in 3 LTCFs to create a model of acute care hospital and LTCF infection control collaboration by developing an LTCF-tailored intervention that reduced infection risk in older adults using MRSA as a proof of concept model. We hypothesized that one can safely remove the MRSA colonization risk from residents of the LTCF in a way that does not interfere with activities of daily living or socialization of residents. This was done by performing a federally registered, prospective, cluster randomized trial in the 3 LTCFs over 2 years (further study information is available from http://clinicaltrials.gov/ct2/ show/NCT01302210?term¼MRSAþinþLongþTermþCare&rank¼1). The strategy involved active surveillance using nasal swab samples, decolonization of carriers on intervention units, hand hygiene instruction, and enhanced cleaning of the environment. This strategy has been used successfully in another trial involving LTCF residents6 and with hospitalized patients in our own facility.2 We hypothesized that this strategy would be successful at lowering MRSA colonization and lead to less infection in this 3-facility LTCF trial. METHODS The study was performed in 12 nursing units at 3 LTCFs that are within 15 miles of each other. The 3 facilities have a combined total of 650-700 beds and 4,200 annual admissions. The units involved were from the following 3 categories: nursing, rehabilitation, and dementia care. The rehabilitation units were composed of mostly short-stay residents. The units at each LTCF were prospectively randomized by a statistician as intervention and nonintervention units. The study activities were carried out in the same manner at all 3 facilities and can be seen in the timeline in Figure 1. Two study nurses coordinated the events at all 3 sites and acted as liaisons with the onsite infection preventionist (IP) and medical director. To determine the burden of MRSA in each facility, 6 point prevalence surveys were conducted to determine if the prevalence of MRSA changed over time. To determine rates of acquisition, 2 periods of admission and discharge testing occurred, and those residents who were polymerase chain reaction (PCR) negative for MRSA on admission and PCR positive, culture positive at discharge were considered to have acquired MRSA. The program began in March 2011 with a point prevalence survey for MRSA nasal colonization at each facility to determine the prevalence of MRSA and identify those already colonized. A team of
study personnel collected a nasal sample from each resident over the course of 1-2 days at each LTCF. After the point prevalence, all residents on the intervention units were given a decolonization regimen of intranasal mupirocin ointment twice a day for 5 days and 1 chlorhexidine bath on the next scheduled bathing day (LTCF standard in Illinois is 1 bath per week). This decolonization regimen was repeated a second time 1 month later (based on preliminary study demonstrating this second decolonization was useful; data not shown). At the same time, in the intervention units, common areas, nursing units, equipment, and patient rooms were thoroughly cleaned with bleach. Hand hygiene education was given to all health care personnel at each LTCF. All admissions subsequent to the point prevalence had a nasal sample collected and tested on site for MRSA colonization within 24 hours. Samples were collected with a double-headed swab in Amies transport solution (Copan, Murrieta, CA). Residents with MRSA-positive nasal screen tests on the intervention units were reported to the nursing staff who then initiated decolonization with the mupirocin-chlorhexidine regimen. Positive patients on the nonintervention units were tested, but results were not reported to the staff, and no further action was taken. Contact isolation precautions were not initiated for any colonized residents in the intervention and nonintervention units at any time during the study. However, it was the policy at each LTCF to place MRSAinfected residents under contact precautions when identified by the infection preventionist as part of routine infection control practice. Point prevalence surveys were performed at 4-month intervals during the first year, along with environmental cleaning of all surfaces. At the end of year 1, for a period of 4 months, residents were screened for nasal MRSA colonization on admission and discharge. The admission and discharge samples provided a paired set of specimens, and the results from these samples were used to determine transmission. Residents that were leaving for home or another institution were sampled on the day of discharge. At the end of year 1, it was realized that during each day all intervention and control residents comingled with each other; therefore, all units were converted to the intervention protocol where all patients received decolonization when the MRSA test was positive. One LTCF continued with mupirocin decolonization; however, 2 others replaced mupirocin with retapamulin because of increasing mupirocin resistance in the MRSA isolates of the residents at these 2 LTCFs. Residents who failed 2 rounds of retapamulin decolonization were offered decolonization with oral rifampin and minocycline,6 with their written consent and the consent of their physician. Discharge testing was once again performed from January to March
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Table 1 MRSA colonization rates from point prevalence data Baseline
Year 1
Year 2
Nasal Screen Tests with MRSA PCR
Intervention
Control
Intervention
Control
Intervention
Control
Number of tests Positive MRSA tests* Culture prevalence (%)
315 53 16.83
358 59 16.48
715 83 11.61
762 136 17.85
1,044 134 12.84
1,230 106 8.62
*Confirmed by culture.
2013, and 2 additional point prevalence surveys occurred at the sixth and twelfth months of year 2. Infection control practices The infection prevention and control program at each LTCF was based on the regulatory requirements for long-term care.7 Prior to the study, infection prevention and control activities included daily informal surveillance and formal weekly infection prevention walking round observation (surveillance). Surveillance information was provided from a 24-hour report that included any resident condition change, culture results, new medications, transfers within the facility, and transfers to and from other health care facilities and the community. Information from formal and informal surveillance was combined with the culture results and antimicrobial prescriptions. The data were compiled and compared with the McGeer et al criteria for documenting an infection in the LTCF.8 A monthly report was completed that included infection rates, outbreak analysis, and quality improvement project results. Contact isolation was initiated when residents had signs and symptoms of an infection caused by a multidrug-resistant organism, Clostridium difficile infection, presence of draining and infected wounds pending culture results, unexplained rashes, nausea, vomiting, diarrhea without another noninfectious explanation, and signs and symptoms of a respiratory illness. Resident and patient rooms and common areas were cleaned daily with a quaternary product. Terminal room cleaning included use of bleach and detergent wipes on all high-touch areas, including toilets and sinks. Bleach and detergent cleaning were used in transmissionbased precautions rooms and all rooms during outbreaks. Statistical analytical methods Differences between time periods were evaluated using the Fisher exact test for proportions. PCR testing The nasal screen test was performed on site at each of the LTCFs with the Xpert MRSA PCR nasal test kit (Cepheid, Sunnyvale, CA). An instrument was placed at each LTCF so samples could be run 24 hours a day, 7 days a week. Either a study nurse or the resident’s nurse was notified that the sample was positive and decolonization could begin. Study personnel retrieved the positive samples and performed a culture on the remnant swab. The remnant swab was plated to a ChromAgar MRSA plate (BD Diagnostic Systems, Sparks, MD), and mauve colonies were subcultured to blood agar for further testing. Colonies resembling S aureus were tested with Staphaurex (Remel, Lenexa, KS) to confirm the identity of MRSA and then tested with an in-house developed PCR assay for the detection of high-level mupirocin resistance.9 The isolates also underwent typing analysis by pulsed-field gel electrophoresis to determine those isolates that were related or identical to each other. Pulsed field gel electrophoresis analysis of MRSA isolates The MRSA isolates were inoculated onto Columbia CNA agar (BD Diagnostic Systems, Sparks, MD) and incubated for 16-24 hours at 37 C. Pulsed-field gel electrophoresis was performed using the
restriction enzyme SmaI, as described previously,10,11 using S aureus NCTC 8325 as a control. Gel images were captured and digitalized as tagged image file format files using a Gel Doc XRþ system with Image Lab Software version 3.0 (Bio-Rad, Hercules, CA), and band comparisons were performed using BioNumerics software version 6.5 (Applied Maths Inc, Austin, TX). Dendrograms were generated for each comparison group using the unweighted pair group method based on arithmetic averages using Dice coefficients. Band tolerance and optimization were set at 1.25% and 0.8%, respectively. Pulsed-field band patterns were considered to be within the same cluster if they had a similarity coefficient 80% and identical if the similarity coefficient was 95%.11,12 This study was approved by the Institutional Review Board at NorthShore University HealthSystem (Protocol EH10-198). RESULTS MRSA nasal colonization rates were determined from the point prevalence surveys and are provided in Table 1. During the baseline period, the colonization rate in tested cultures was 16.64%. During year 1 of the study, the colonization rate was reduced to 11.61% in the intervention units (P ¼ .028) but remained stable at 17.85% in the control units (P ¼ .613) compared with baseline. The difference in rate between the intervention and control units was statistically significant (P ¼ .001). During year 2, when all units received the intervention, the colonization rate was 10.55%. The difference between baseline and year 2 was statistically significant (P < .001). Conversion rates were based on paired admission and discharge testing samples where the admission screen test was negative and the discharge screen was a PCR-positive, culture-positive test (Table 2). From year 1 to year 2, a significant increase in the transmission rate was observed, along with a smaller, nonsignificant increase in the admission prevalence. This change is driven primarily by the large and statistically significant changes in LTCF 1. Admission prevalence remained stable at LTCFs 2 and 3. Most conversions occurred on short-term stay units. For LTCF 1, 7 of 12 conversions were on short-term units. The average length of stay (LOS) for short-term unit conversions was 28 days; for long-term unit conversions it was 32 days. For LTCFs 2 and 3, 92% and 93% of conversions were on short-term units, respectively. The average LOS for a conversion on a short-term unit at LTCF 2 was 17.5; for LTCF 3 it was 28 days. The only long-term stay conversion at LTCF 2 was at 152 days; for LTCF 3, the conversion was at 42 days. The average LOS for short-term and long-term units at each facility during the course of the study can be found in Table 3. MRSA nasal isolates were available for molecular typing in 36 of the 39 residents who acquired MRSA as a result of transmission. In 22 of the 36 isolates, there was an identifiable, potential source of MRSA as evidenced by geographic proximity of the recipient isolate to a closely related or identical isolate. In 1 LTCF, identifiable isolates identical to those acquired could be traced to residents housed in rooms next to each other. Additionally, the results of PCR testing for mupirocin resistance can be found in Table 4.
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Table 2 Acquisition rates according to discharge testing during 1 quarter per study year Facility Total Number of residents sampled on admission Positive cultures on admission Admission prevalence (%) Number of residents sampled on discharge Culture negative on admission and positive at discharge Acquisition rate (%) LTCF 1 Number of residents sampled on admission Positive cultures on admission Admission prevalence (%) Number of residents sampled on discharge Culture negative on admission and positive at discharge Acquisition rate (%) LTCF 2 Number of residents sampled on admission Positive cultures on admission Admission prevalence (%) Number of residents sampled on discharge Culture negative on admission and positive at discharge Acquisition rate (%) LTCF 3 Number of residents sampled on admission Positive cultures on admission Admission prevalence (%) Number of residents sampled on discharge Culture negative on admission and positive at discharge Acquisition rate (%)
Year 1
Year 2
P value
1,708 58 3.40 725 12
1,206 50 4.15 767 27
.32
1.66
3.52
.034
543 7 1.29 205 1
395 15 3.80 271 11
.015
0.49
4.06
.016
720 16 2.22 324 6
509 13 2.55 304 9
.707
1.85
2.96
.438
445 35 7.87 196 5
302 22 7.28 192 7
.888
2.55
3.65
.572
Table 4 Mupirocin resistance rates in MRSA isolates found on admission to the 3 long-term care facilities Facility
Table 3 Average length of stay for long-term and short-term stay units at each long-term care facility Facility
Short-term stay unit
Long-term stay unit
LTCF 1 LTCF 2 LTCF 3
25 days 17.5 days 26 days
187 days 306 days 13 years
DISCUSSION In 2005, our health care system instituted universal admission screening for nasal colonization with MRSA.2 At that time we discovered that a large number of MRSA colonized patients entering our hospitals were from local LTCFs. Surgical patients are sent to rehabilitate in these LTCFs, making us part of the same health care team. Collaboration with the LTCFs on the reduction of MRSA colonization seemed like a natural next step. We reached out to LTCFs in the area and found willing partners. One LTCF outside of our health care system also requested participation. We began a demonstration project to create a model of hospital to LTCF infection control collaboration using the prevention of MRSA as a proof of concept model. Our goal was to develop LTCF-tailored interventions that reduced colonization and infection risk in older adults. An aim of the project was to show that one can safely remove the MRSA colonization risk from the residents in a way that does not affect their home-like style of living. The strategy involved some techniques that are typical in a hospital infection control program (eg, nasal surveillance testing, decolonization strategies, hand hygiene education, enhanced environmental cleaning regimens) but avoided other practices (eg, contact isolation practices for MRSA colonization). Nasal surveillance testing was performed on site at each LTCF by either a nurse or the study personnel using
LTCF 1 (%) LTCF 2 (%) LTCF 3 (%)
Year 1
Year 2
15.4 14.8 2.5
2.4 15.1 2.8
the Xpert MRSA PCR test. This assay is simple to perform, needs minimal supplies, has a small instrument footprint, and results are available within 1 hour. In this research project, nurses performed routine quality control and patient testing for the 2-year study without incident, and testing was easily implemented at the LTCF. Our results indicate that there was no difference in the MRSA prevalence rates when comparing intervention and control units at baseline, but statistical significance was seen in the intervention unit compared with baseline and from years 1 and 2 (Table 1). Because no other changes were implemented at the LTCF, the improvement was likely the result of the intervention. LOS of the residents at the time of acquisition had no effect because most conversions were on short-term stay units and their LOS was similar with the average at each LTCF. The MRSA acquisition increased somewhat from year 1 to year 2, and this increase was statistically significant (Table 2). It is unexplained and important that the increase did not impact the overall MRSA prevalence. In a recent report by Jones et al4 studying 1.4 million patient admissions in 112 hospitals in the Veterans Administration health care system, the authors found that a patient colonized or infected on admission imports MRSA into the hospital, and this admission prevalence contributes to the transmission risk. This investigation demonstrated that a 10% increase in a hospital’s average admission prevalence was associated with a 9.7% increase in the weekly acquisition rate.4 We did see an MRSA admission prevalence increase at LTCF 1 during discharge testing in year 2, and it was associated with a significant increase in transmission at LTCF 1, but this was not seen at the other facilities. This LTCF was the sole driver for the increase in the total acquisition rate. Although we have no explanation for the increase in MRSA-positive admissions at LTCF 1, it may explain an increase in acquisition rates and correlates with what was seen in the Veterans Administration report.4 Of interest was the need for the use of retapamulin for decolonization in year 2, which is understandable because 2 of the LTCFs (LTCFs 1 and 2) send their sick residents to hospitals that are within our health care system (and the third does not); during the period of this study, NorthShore was routinely decolonizing MRSApositive inpatients with mupirocin that had led to a mupirocin resistance rate in MRSA exceeding 10%. Therefore, LTCFs 1 and 2 likely had a higher rate of mupirocin resistance in their MRSA admission isolates in year 1 (Table 3) because of the rising resistance in our health care system.13 Therefore, in the second year of the study, residents of LTCFs 1 and 2 received retapamulin as a decolonization agent in place of mupirocin to maximize the success of the decolonization regimen. Critical to our research program, active surveillance, decolonization, and cleaning regimens did not appear to interrupt activities of daily living for the residents of the 3 LTCFs. There were no complaints by any residents, family, or staff about any components of this 2-year study. There are a few limitations to this research. Discharge testing was limited to 25% of the study period and involved mostly shortterm stay residents. If we had included residents who were negative at 1 point prevalence and positive at the next, it might have given us a broader picture of transmission at these LTCFs, but these activities did not capture all the residents staying in the LTCFs for the entire year; therefore, no accurate statistical assessment could
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be made. Another potential limitation involved results from a project evaluating surveillance of MRSA colonization from 5 different body sites.14 Sites that were sampled included the nose, axilla, throat, perineum, and perianal areas. Only 81% of the residents sampled that were colonized with MRSA somewhere on their body were also colonized in their nose. Although we believe that nasal surveillance was sufficient for determining the prevalence of MRSA at the LTCF, it is possible that residents colonized at other sites may significantly contribute to MRSA spread and would not have been captured. Finally, not measuring LOS as a risk factor for MRSA acquisition is another potential limitation. However, this is a well-known risk factor and we were not studying risks for MRSA acquisition but rather whether colonization prevalence could be reduced. Studying LOS as a risk factor would require another research approach (eg, weekly nasal screening), something beyond the scope of this investigation. CONCLUSION The planned interventions of screening and decolonization were successful at lowering MRSA colonization in LTCF residents. A rise in MRSA transmission did not reverse this trend. The study interventions did not interrupt activities of daily living for the residents and could be implemented in other LTCFs. In-house (LTCF) PCR for MRSA was easily accomplished by nursing personnel and could be part of a comprehensive LTCF MRSA decolonization program, with testing done either before admission or at the time of entry into an LTCF. This collaboration between acute and long-term care resulted in an ongoing relationship between the acute care system and LTCF involved in the project. References 1. Reynolds C, Quan V, Kim D, Peterson E, Dunn J, Whealon M, et al. Methicillinresistant Staphylococcus aureus (MRSA) in 10 nursing homes in Orange County, California. Infect Control Hosp Epidemiol 2011;32:91-3.
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2. Robicsek A, Beaumont JL, Paule SM, Hacek DM, Thomson RB Jr, Kaul KL, et al. Universal surveillance for methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals. Ann Intern Med 2008;148:409-18. 3. Ridgway J, Peterson L, Brown E, Du H, Hebert C, Thomson R, et al. Clinical significance of methicillin-resistant Staphylococcus aureus colonization on hospital admission: one-year infection risk. PLoS One 2013;8:e79716. 4. Jones M, Ying J, Huttner B, Evans M, Maw M, Nielson C, et al. Relationships between the importation, transmission and nosocomial infections of methicillin-resistant Staphylococcus aureus: an observational study of 112 Veterans Affairs medical centers. Clin Infect Dis 2014;58:32-9. 5. Capitano B, Lesham OA, Nightingale CH, Nicolau DP. Cost effect of managing of methicillin-resistant Staphylococcus aureus in a long-term care facility. J Am Geriatr Soc 2003;51:10-6. 6. Bowler WA, Bresnahan J, Bradfish A, Fernandez C. An integrated approach to methicillin-resistant Staphylococcus aureus control in a rural, regional-referral healthcare setting. Infect Control Hosp Epidemiol 2010;31:269-75. 7. Department of Health & Human Services; Centers for Medicare and Medicaid Services (CMS) Tag F441. CMS manual system Pub. 100-07 state operations provider certification. Available from: https://www.cms.gov/Regulations-andGuidance/Guidance/Transmittals/downloads/r51soma.pdf. Accessed July 20, 2009. 8. McGeer A, Campbell B, Emori T, Hierholzer W, Jackson M, Nicolle L, et al. Definitions of infection for surveillance in long-term care facilities. Am J Infect Control 1991;19:1-7. 9. Hacek DM, Robb WJ, Paule SM, Kudrna JC, Stamos VP, Peterson LR. Staphylococcus aureus nasal decolonization in joint replacement surgery reduces infection. Clin Orthop Relat Res 2008;466:1349-55. 10. Jaggi P, Paule SM, Peterson LR, Tan TQ. Characteristics of Staphylococcus aureus infections, Chicago Pediatric Hospital. Emerg Infect Dis 2007;13: 311-4. 11. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, Tenover FC. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 2003;41:5113-20. 12. Limbago B, Fosheim GE, Schoonover V, Crane CE, Nadle J, Petit S, et al. Characterization of methicillin-resistant Staphylococcus aureus isolates collected in 2005 and 2006 from patients with invasive disease: a population-based analysis. J Clin Microbiol 2009;47:1344-51. 13. Dusich IK, Schora D, Peterson LR, Thomson RB Jr. Analysis of mupirocin susceptibility in a hospital setting utilizing mupirocin for decolonization of patients with nasal carriage of MRSA or MSSA. Proceedings of the 113th General Meeting of the American Society for Microbiology, 2013 May, 18-21, Denver, CO. 14. Schora DM, Boehm S, Das S, Patel PA, Schora K, Peterson KE, et al. Detection of methicillin-resistant Staphylococcus aureus (MRSA) from multiple body sites of residents at long-term care facilities. Advances in the Prevention and Control of Healthcare-Associated Infections. Available at: http://www.ahrq. gov/professionals/quality-patient-safety/patient-safety-resources/resources/ advances-in-hai/index.html. Accessed August 14, 2014.