Mandatory MRSA Screening: Mixed Results Fuel the Ongoing Debate Over Its Value

Article

Screening patients for methicillin-resistant Staphylococcus aureus (MRSA) has become a controversial topic causing heated debate. In fact, many healthcare professionals consider the question of whether to test patients for MRSA before admission to be one of the most compelling issues in modern healthcare.

By Elizabeth Srejic

Screening patients for methicillin-resistant Staphylococcus aureus (MRSA) has become a controversial topic causing heated debate.1 In fact, many healthcare professionals consider the question of whether to test patients for MRSA before admission to be one of the most compelling issues in modern healthcare.2

MRSA screening programs are mandated by various governmental agencies and much of the literature supports their continued use. However, a comparable number of studies find screening programs to be ineffective and not congruent with evidence-based medicine, and the literature has raised questions about populations appropriate for screening, screening methods, subsequent interventions, and cost, among others.3-6 Some authorities also criticize MRSA screening for being a vertical infection control approach, a relatively narrow tactic that aims to eradicate a single type of pathogen, instead of a horizontal approach, a broader method designed to wipe out many types of pathogens, and say screening is only effective when practiced in conjunction with other infection control interventions in a bundle with such elements as hand hygiene, antibiotics stewardship, decolonization of carriers and institutional culture change.

Rates of healthcare associated infections (HAIs) caused by antibiotic-resistant bacteria remain high in the United States and HAIs are the most common complication during inpatient hospital care.7 According to Demirjian et al. (2015) in a Morbidity and Mortality Weekly Report published by the Centers for Disease Control and Prevention (CDC): “Each year in the United States, approximately two million persons become infected with antibiotic-resistant bacteria, at least 23,000 persons die as a direct result of these infections, and many more die from conditions complicated by a resistant infection. Antibiotic-resistant infections contribute to poor health outcomes, higher healthcare costs, and use of more toxic treatments. Although emerging resistance mechanisms are being identified and resistant infections are on the rise, new antibiotic development has slowed considerably. “

Of the known antibiotic-resistant bacteria, MRSA has emerged as a predominant cause of HAIs.8-9 Eighty-six percent of the 94,360 invasive MRSA infections that occur annually in the United States are HAIs and 18,650 of these cases result in death.10 Treatment options for MRSA are limited and less effective than options available for susceptible S. aureus infections and result in higher morbidity and mortality, and the high prevalence of unfavorable antibiotic prescribing contributes to further spread of resistance.11

In most MRSA screening programs, also called active surveillance programs, a patient population is tested for MRSA at admission – even when showing no signs of active infection –and then isolated and possibly subjected to other interventions.12-13 To inhibit MRSA transmission, healthcare workers (HCW) may use standard or contact precautions such as hand hygiene, patient isolation, and personal protective equipment (PPE) with known carriers who may further receive decolonization therapy with topical antibiotics like mupirocin or chlorhexidine-gluconate (CHG) baths in an attempt to make them non-carriers.14-15 As opposed to testing all patients, targeted screening is a more focused approach that tests only specified higher-risk groups such as intensive care unit (ICU) or emergency department (ED) patients or those with histories of MRSA infection.16

Research surrounding MRSA screening continues to show mixed results, with studies reporting successful MRSA screening in some but not all settings or that it may or may not be costly, and that it may or may not require ancillary interventions to be successful.17-18 Asymptomatic MRSA carriers are at risk of contracting MRSA infections – for example, the risk of surgical site infections (SSI) is approximately 30-fold higher in these patients – and the spread of MRSA is facilitated in healthcare environments19 –  but the literature still fails to establish whether identifying and isolating persons colonized with MRSA reduces the incidence of subsequent MRSA infection.20 Due to the lack of high-quality, definitive re-search, many experts therefore say the case for active surveillance is weak and backed by low strength of evidence.21

However, positive studies on MRSA screening have shown that the practice successfully lowers the incidence of MRSA HAIs, or at least effectively identifies MRSA carriers who may be at high risk for transmitting MRSA or developing infectious complications, in inpatient rehabilitation facilities, ICUs, nursing homes, emergency departments (EDs) and other facilities.22-24 On the other hand, contrary studies designed with similar parameters say MRSA screening is ineffective.25 Other common study findings are that screening is only effective in certain settings or when included in a bundle of infection control interventions that make it difficult to evaluate the efficacy of screening alone.26-28 Some studies have also concluded that hospitals should focus on preventative measures rather than screening.29 “Screening programs for MRSA colonization are expensive and of dubious utility,” Parks and Croce wrote in a review (2002). “Standard infection control practices, diligent hand hygiene, and careful antimicrobial stewardship remain the tenets of prevention of MRSA infections.”30

An observational study by Robicsek et al. (2008) found that introduction of universal admission surveillance for MRSA in a three-hospital, 850-bed organization with approximately 40,000 annual admissions was associated with a large reduction in MRSA disease during admission and 30 days after discharge.31 The study compared rates of MRSA clinical disease during and after hospital admission in three consecutive periods: a baseline period during which no MRSA surveillance was performed, a 12-month period of targeted MRSA screening among patients being ad-mitted to the ICU, and a 21-month period of universal MRSA screening. Rapid polymerase chain reaction (PCR) testing of the nares was used to identify carriers who were then subjected to contact isolation and topical decolonization therapy. The researchers used statistical models to compare prevalence density of MRSA infections in several body sites, during each period, with the bloodstream used as a control, and during the period of universal surveillance the prevalence density of MRSA infection at each body site statistically significantly decreased compared with the baseline period. The MRSA disease rate also decreased during hospitalization and in the 30 days after discharge although no further reduction occurred thereafter.

Another study describing lowered HAI rates in conjunction with MRSA screening, a quasi-experimental, interrupted time-series by Lee, et al. (2005), reported that an active screening and decolonization program was independently associated with a decrease in MRSA HAIs after adjust-ing for confounding variables; the MRSA infection rate decreased from 3.58 percent at baseline to 0.18 percent when the intervention period ended.32 Likewise, Huang and colleagues (2006) reported that routine surveillance for MRSA in eight ICUs in an 800-bed hospital allowed earlier initiation of contact isolation precautions and was associated with large and statistically significant reductions in the incidence of MRSA bacteremia in the ICUs and hospital wide.33 And Win, et al. found a targeted screening and isolation program reduced the HAI acquisition rate in a hospital by 1.6 percent.34

One population that MRSA screening has particularly aided is patients undergoing various types of surgery, by lowering the incidence of SSIs.35-39 Conversely, Harbarth, et al. (2008) reported in the Journal of the American Medical Association that a universal, rapid MRSA admission screening strategy did not reduce MRSA HAIs in a surgical department.40 In the prospective, interventional cohort study, 515 MRSA-positive patients (5.1 percent), including 337 previously unknown MRSA carriers were identified in the screening of 10,193 patients (94 percent). During the screening period, 93 patients developed nosocomial MRSA infection compared with 76 in the control periods and the rate of MRSA SSI and nosocomial MRSA acquisition did not change significantly. Fifty-three of 93 infected patients (57 percent) in the intervention wards were MRSA-free on admission and developed MRSA infection during hospitalization.

Instead of reporting HAI rates after implementing infection control programs with MRSA screening, numerous studies in the literature focus on comparing screening methods. One example is a prospective, interventional study by Leonhardt, et al. (2011) which found that universal screening, in comparison with targeted screening, increased the rate of MRSA detection upon hospital admission but did not significantly reduce the rate of MRSA HAIs.41 Ziakas, et al (2015) reported universal decolonization was the most superior of tested screening and intervention combinations, averting 1.31 percent and 1.59 percent of MRSA infections over targeted decolonization and screening and contact precautions, respectively.42 Furthermore, Huang, et al. (2013) in a study published in the New England Journal of Medicine and funded by the CDC reported that in routine ICU practice universal decolonization was more effective than targeted decolonization or screening and isolation in reducing rates of MRSA clinical isolates and bloodstream infection from any pathogen.43 And Roth, et al. (2015) found the introduction of universal MRSA ad-mission screening did not significantly affect MRSA HAI rates compared with targeted screening.44
Contributing to the abundance of conflicting results in the literature, some studies only recommend screening when it is practiced with sub-sequent decolonization or other infection control interventions in a bundle.45-49

Decolonization has shown mixed results and emerging resistance to decolonization agents such as mupirocin and CHG is a significant con-cern.50-51 For example, Dow, et al. (2010) found MRSA decolonization in hospitalized patients can be beneficial over the short- and long-term when used in a multifactorial approach including CHG bathing, enhanced hygiene and housekeeping, and combination oral/topical antimicrobial therapy,52 and Gebreselassie, et al. in a systematic review and meta-analysis found using mupirocin together with whole-body decolonization was highly effective in eradicating MRSA carriage in hemodialysis patients.53 Conversely, Landelle, et al. (2015) found no significant difference in MRSA colonization between patients treated with a topical antibiotic applied to the anterior nares and skin and patients treated with placebo after 28 days of treatment,54 and Bellini, et al. (2015) reported decolonization after universal screening of carriers along with routine standard precautions did not significantly reduce the prevalence of MRSA carriage at one year compared with standard precautions alone.55

Regarding the question of decolonization, Kirk Huslage, RN, BSN, MSPH, CIC, vice chair of the Association for Professionals in Infection Control and Epidemiology (APIC) Public Policy Committee, associate director of North Carolina Statewide Infection Control and Epidemiology (SPICE), agreed with the negative findings: “There is a lot of evidence that decolonization has not been demonstrated to be effective, with insufficient evidence that topical or systemic antimicrobial therapy is effective for eradicating nasal or extra-nasal carriage of MRSA. And when you’re applying an antibiotic to rid someone of MRSA, you’re increasing the likelihood of resistance. In the short term it might clear someone’s MRSA but they can become recolonized.”

Regarding the efficacy of bundling, Lee, et al. (2013) found that combined approaches to reduce rates of MRSA HAIs including enhancing standard precautions and MRSA-specific infection control interventions were required to reduce MRSA rates, whereas single interventions were not effective except in clean surgery wards where MRSA screening coupled with contact precautions and decolonization was associated with significant reductions in MRSA clinical culture and infection rates.56 Similarly, Widmer, et al. (2015) found that a bundled program including strict contact precautions with single rooms for MRSA-colonized or -infected patients, targeted admission screening of high-risk patients and healthcare workers at risk for carriage, molecular typing of all MRSA strains and routine decolonization of MRSA carriers including healthcare workers was effective as assessed by the incidence of MRSA bloodstream infections.57 The researchers concluded long-term control of MRSA is feasible when a bundle of infection control precautions is strictly enforced over time. And Chalfine, et al. (2012) in a multifaceted hospital-wide prevention program including active screening and decontamination of ICU patients, hospital wide use of alcohol-based handrubs, antibiotics stewardship, compliance audits, and feedback provided  to care providers reported lowered  MRSA HAI colonization and use of antibiotics.58
In lieu of a screening program, some experts recommend a preventive approach to MRSA control by simply reinforcing or increasing standard precautions.59 Using standard or contact precautions has successfully lowered the incidence of MRSA HAIs when practiced alone or as part of a bundle of infection control interventions.60-64 For example, Kullar, et al. (2015) found using contact precautions reduced MRSA transmission in epidemic settings and in instances with high compliance although it failed to lower MRSA HAI rates.65 Kullar, et al. added that unintended con-sequences of contact precautions include decreased HCW time spent with patients, low HCW compliance, decreased perceptions of comfort from patients, and greater likelihood of patient complaints and negative psychological implications. In addition, on these unintended consequences, Barratt, et al. (2011) wrote in a review that source isolation may result in detrimental psychological effects including anxiety, stress and depression, and may also lead to the patient receiving less or substandard care.66

Huslage says that multi-modal bundles of interventions including standard precautions are the most effective approach to MRSA control: “A lot of data has shown that MRSA can be adequately controlled without universal or targeted screening by using bundles potentially composed of environmental cleaning, hand hygiene, CHG bathing, use of PPE, disinfection of surfaces and equipment, and antibiotic stewardship. All of those are horizontal interventions that can have a dramatic impact on MRSA rates as well as other rates of infections. Horizontal interventions are superior to vertical approaches like MRSA screening as they can control for several pathogens rather than just MRSA -- they’re multi-potent. A horizontal population-based approach really maximizes resources to make the biggest impact across all the pathogens and all of the HAI spectrums. MRSA HAIs cause approximately 10 percent of HAIs in the U.S. and the remaining 90 percent of other bacterial infections are just as serious and just as important and they are best controlled by horizontal measures.”

Economic considerations are another important factor to consider in the decision to implement, maintain, or discontinue active surveillance systems in healthcare settings.67 Confusingly, MRSA screening programs have been called expensive and labor intensive in the literature,68 while some studies assert that they require minimal time69 and eventually save money.70

Lee, et al. (2005) indicated that MRSA screening is cost-effective in an analysis of a targeted screening program in a surgical ICU, reporting that $22 in medical costs can be saved for every $1 spent on an intervention.71 Farbman, et al. (2013) in a systematic review of both universal and targeted screening programs with conventional and PCR-based testing reported favorable cost/benefit and save/cost ratios as well as a median cost per month of $8,648 and median savings of $38,751.72 And Shenov, et al. (2015) in a prospective cohort study of PCR-based screening and discontinuation of MRSA contact precautions in an ED found that predicted revenue exceeded predicted program costs.73

On the other hand, McKinnell, et al. (2015) in estimating the direct economic impact of initiating a universal MRSA screening and contact precautions program in a hospital discovered that testing increased the economic costs of the screening program although it did identify more MRSA-colonized persons and avert more MRSA HAIs.74 “We found that universal MRSA screening, although providing potential benefit in pre-venting MRSA infection, is relatively costly and may be economically burdensome for a hospital,” the authors wrote. “Policymakers should con-sider the economic burden of MRSA screening and contact precautions in relation to other interventions when choosing programs to improve patient safety and outcomes.”

Also, Garcia, et al. (2011) in a study examining cost and health outcomes associated with mandatory MRSA screening in a pediatric special care nursery wrote:  “Mandatory screening leads to increased costs, problems related to false-positives, and unintended consequences (e.g., decision whether to treat non-MRSA organisms identified on screening cultures, possibility of legal implications, adverse family psychosocial effects, and questionable validity of the PCR test). The average total costs of laboratory, supply, and personnel were $15,270.12 ($34.31 per infant or $19.58 per screen).”75

One way to reduce the cost of MRSA screening is to use traditional swab culturing, which is slower but less costly than PCR-based methodol-ogy, which is faster and more accurate than conventional testing but also more expensive.76 Another way may be to implement targeted screening programs rather than universal screening of large populations; the may be less expensive,77-80 although the latter may detect more cases of MRSA.81 

High costs involved in MRSA testing have raised concerns over laws requiring mandatory screening. Accordingly, the APIC indicated it opposes such legislation in a joint position statement with the Society for Healthcare Epidemiology of America (SHEA) released in 2007.82

Huslage agrees: “Legislation requiring mandatory MRSA screening puts additional burden on facilities that are under-funded and does not provide them with the additional resources necessary to provide that kind of data and implement those kinds of controls and interventions. Generally, legislation is not sufficiently flexible to permit a rapid response to local epidemiologic trends and changes in the way that microbial resistance is developing in a hospital. Infection control should allow for analyzing local trends and making a determination on what is of greatest concern at that local level, rather than detracting from hospital control at the local level and possibly preventing appropriation of limited re-sources toward more pressing issues.”

Although significant progress has been made in identifying interventions that may be effective in preventing transmission of multidrug-resistant organisms in healthcare settings, the exact and relative importance of different infection control measures remain under investigation.83  Nonetheless, healthcare facilities should draw up and implement infection control practices.84 Successful MRSA prevention and control requires concerted efforts, and facilities should consider an array of strategies as well as their individual characteristics, budget and program outcomes, in developing and maintaining their MRSA infection control program.85-86

Elizabeth Srejic is a freelance writer.

MRSA Screening: Q&A with Frank Myers

By Elizabeth Srejic

Frank Myers, MA, CIC, an infection preventionist with the UC San Diego Health System, provides his perspective on MRSA screening.

Q: What are the specifics of your facility’s methicillin-resistant Staphylococcus aureus (MRSA) screening program?
A: We comply with California law which requires methicillin-resistant Staphylococcus aureus (MRSA) screening of individuals who are being admitted to the ICU, coming from long-term care facilities, getting dialysis or for other reasons. However, we do not actively place MRSA patients or the area patients in standard precautions anymore as we’ve become convinced by literature showing that institutions that never screened or stopped screening patients saw no increase in their rates of and other literature that suggests that the more patients you have in contact precautions the less effective precautions become.

Q: How has your MRSA screening program affected your rates of MRSA healthcare acquired infections (HAIs)?
A: When mandatory screening was actually implemented in this state, I was with a different system. We were actively placing patients in standard precautions there and when screening was implemented we found more cases of MRSA but certainly did not see any changes in our transmission rates which were already pretty low. In my current institution, we were also placing patients in standard precautions and when we added mandatory screening we likewise saw no reduction in transmission rates which were similarly low. So basically the law had no impact on us in either case other than expenditure of money on our screening program. And this has actually been reproduced in a number of poster presentations throughout many states where mandatory active surveillance was passed.

Q: Why do you think that some studies show that MRSA screening programs can be successful in lowering MRSA infection rates?
A: I think that all of us agree that in outbreak situations active surveillance as a short-term intervention designed to control the outbreak makes sense. Over the long term, however, active surveillance is not as effective as other interventions in lowering rates of infection.

Q: Some studies say MRSA screening programs are not cost effective whereas other studies insist that they save a lot of money over the long run.  What aspects of MRSA screening programs make them expensive?
A: MRSA screening programs entail costs such as personnel and laboratory hours and personal protective equipment (PPE). Allocating money to these becomes even more expensive over the long run since reports indicate that MRSA screening programs fail to lower infection rates and MRSA infection rates do not increase when institutions discontinue their screening programs.

Q: Are front-end strategies like hand hygiene and CHG-bathing better than a screening program?
A: Studies have shown these and other horizontal approaches which can eradicate many types of pathogens instead of just one type of pathogen are more successful than MRSA-specific strategies in controlling MRSA. These broader approaches are more effective in interrupting disease transmission than narrower search-and-destroy methods and I think that they are where the future of prevention efforts lies.

References:

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10. Ibid.
11. Ibid.
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44. Roth VR, Longpre T, Taljaard M, Coyle D, Suh KN, Muldoon KA, Ramotar K, Forster A. Universal vs Risk Factor Screening for Methicillin-Resistant Staphylococcus aureus in a Large Multicenter Tertiary Care Facility in Canada. Infect Control Hosp Epidemiol. 2015 Oct 16:1-8. [Epub ahead of print]
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47. Huang SS, Septimus E, Kleinman K, Moody J, Hickok J, Avery TR, Lankiewicz J, Gombosev A, Terpstra L, Hartford F, Hayden MK, Jernigan JA, Weinstein RA, Fraser VJ, Haffenreffer K, Cui E, Kaganov RE, Lolans K, Perlin JB, Platt R; CDC Prevention Epicenters Program; AHRQ DECIDE Network and Healthcare-Associated Infections Program. Targeted versus universal decolonization to prevent ICU infection. N Engl J Med. 2013 Jun 13;368(24):2255-65. doi: 10.1056/NEJMoa1207290. Epub 2013 May 29.
48. Ziakas PD, Zacharioudakis IM, Zervou FN, Mylonakis E. Methicillin-resistant Staphylococcus aureus prevention strategies in the ICU: a clinical decision analysis*. Crit Care Med. 2015 Feb;43(2):382-93. doi: 10.1097/CCM.0000000000000711.
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53. Gebreselassie HM, Lo Priore E, Marschall J. Effectiveness of meticillin-resistant Staphylococcus aureus decolonization in long-term haemodialysis patients: a systematic review and meta-analysis.  J Hosp Infect. 2015 Nov;91(3):250-6. doi: 10.1016/j.jhin.2015.08.015. Epub 2015 Aug 29.
54. Landelle C, von Dach E, Haustein T, Agostinho A, Renzi G, Renzoni A, Pittet D, Schrenzel J, François P, Harbarth S. Randomized, placebo-controlled, double-blind clinical trial to evaluate the efficacy of polyhexanide for topical decolonization of MRSA carriers.J Antimicrob Chemother. 2015 Oct 27. pii: dkv331. [Epub ahead of print]
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56.  Lee AS, Cooper BS, Malhotra-Kumar S, Chalfine A, Daikos GL, Fankhauser C, Carevic B, Lemmen S, Martínez JA, Masuet-Aumatell C, Pan A, Phillips G, Rubinovitch B, Goossens H, Brun-Buisson C, Harbarth S; MOSAR WP4 Study Group. Comparison of strategies to reduce meticillin-resistant Staphylococcus aureus rates in surgical patients: a controlled multicentre intervention trial. BMJ Open. 2013 Sep 19;3(9):e003126. doi: 10.1136/bmjopen-2013-003126.
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60. Ibid.
61. Ibid.
62. Jain R, Kralovic SM, Evans ME, Ambrose M, Simbartl LA, Obrosky DS, Render ML, Freyberg RW, Jernigan JA, Muder RR, Miller LJ, Roselle GA. Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. N Engl J Med. 2011 Apr 14;364(15):1419-30. doi: 10.1056/NEJMoa1007474.
63. Lee AS, Cooper BS, Malhotra-Kumar S, Chalfine A, Daikos GL, Fankhauser C, Carevic B, Lemmen S, Martínez JA, Masuet-Aumatell C, Pan A, Phillips G, Rubinovitch B, Goossens H, Brun-Buisson C, Harbarth S; MOSAR WP4 Study Group. Comparison of strategies to reduce meticillin-resistant Staphylococcus aureus rates in surgical patients: a controlled multicentre intervention trial. BMJ Open. 2013 Sep 19;3(9):e003126. doi: 10.1136/bmjopen-2013-003126.
64. Jacobs A.Hospital-acquired methicillin-resistant Staphylococcus aureus: status and trends. Radiol Technol. 2014 Jul-Aug;85(6):623-48; quiz 649-52.
65. Am J Infect Control. 2015 Sep 12. pii: S0196-6553(15)00850-0. doi: 10.1016/j.ajic.2015.08.003. [Epub ahead of print]
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68. Ibid.
69. Peterson LR, Diekema DJ. To screen or not to screen for methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2010 Mar;48(3):683-9. doi: 10.1128/JCM.02516-09. Epub 2010 Jan 13.
70. Win MK, Soliman TA, Lee LK, Wong CS, Chow A, Ang B, Roman CL, Leo YS. Review of a two-year methicillin-resistant Staphylococcus aureus screening program and cost-effectiveness analysis in Singapore. BMC Infect Dis. 2015 Sep 29;15:391. doi: 10.1186/s12879-015-1131-5.
71. Lee YJ, Chen JZ, Lin HC, Liu HY, Lin SY, Lin HH, Fang CT, Hsueh PR. Impact of active screening for methicillin-resistant Staphylococcus aureus (MRSA) and decolonization on MRSA infections, mortality and medical cost: a quasi-experimental study in surgical intensive care unit. Crit Care. 2015 Apr 8;19:143. doi: 10.1186/s13054-015-0876-y.
72. Farbman L, Avni T, Rubinovitch B, Leibovici L, Paul M. Cost-benefit of infection control interventions targeting methicillin-resistant Staphylococcus aureus in hospitals: systematic review. Clin Microbiol Infect. 2013 Dec;19(12):E582-93. doi: 10.1111/1469-0691.12280. Epub 2013 Aug 28.
73. Shenoy ES, Lee H, Cotter JA, Ware W, Kelbaugh D, Weil E, Walensky RP, Hooper DC. Impact of rapid screening for discontinuation of methicillin-resistant Staphylococcus aureus contact precautions.Am J Infect Control. 2015 Oct 1. pii: S0196-6553(15)00936-0. doi: 10.1016/j.ajic.2015.08.019. [Epub ahead of print]
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76. Parks NA, Croce MA. Routine screening for methicillin-resistant Staphylococcus aureus. Surg Infect (Larchmt). 2012 Aug;13(4):223-7. doi: 10.1089/sur.2012.130. Epub 2012 Aug 22.
77. Ibid.
78. Ibid.
79. Collins J, Raza M, Ford M, Hall L, Brydon S, Gould FK. Review of a three-year meticillin-resistant Staphylococcus aureus screening programme. J Hosp Infect. 2011 Jun;78(2):81-5. doi: 10.1016/j.jhin.2011.02.012. Epub 2011 Apr 20.
80. Tübbicke A, Hübner C, Hübner NO, Wegner C, Kramer A, Fleßa S. Cost comparison of MRSA screening and management - a decision tree analysis. BMC Health Serv Res. 2012 Dec 1;12:438. doi: 10.1186/1472-6963-12-438.
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82. Weber SG, Huang SS, Oriola S, Huskins WC, Noskin GA, Harriman K, Olmsted RN, Bonten M, Lundstrom T, Climo MW, Roghmann MC, Murphy CL, Karchmer TB. Legislative mandates for use of active surveillance cultures to screen for methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci: Position statement from the Joint SHEA and APIC Task Force. Am J Infect Control. 2007 Mar;35(2):73-85.
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84. Spagnolo AM, Orlando P, Panatto D, Amicizia D, Perdelli F, Cristina ML. Staphylococcus aureus with reduced susceptibility to vancomycin in healthcare settings. J Prev Med Hyg. 2014 Dec;55(4):137-44.
85. Peterson LR, Diekema DJ. To screen or not to screen for methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2010 Mar;48(3):683-9. doi: 10.1128/JCM.02516-09. Epub 2010 Jan 13.
86. Kock R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J, Mielke M, Peters G, Skov RL, Struelens MJ, Tacconelli E, Witte W, Friedrich AW. Systematic literature analysis and review of targeted preventive measures to limit healthcare-associated infections by meticillin-resistant Staphylococcus aureus. Euro Surveill. 2014 Jul 24;19(29). pii: 20860.

 

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