Nurse Education Today 30 (2010) 789–793
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Nurse Education Today j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / n e d t
Assessing methicillin-resistant Staphylococcus aureus knowledge among nursing students Andrea Jennings-Sanders ⁎, Lucy Jury Louis Stokes Cleveland Department of Veterans Affairs Medical Center, 10701 East Boulevard, Cleveland, OH 44106, USA
a r t i c l e
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Article history: Accepted 23 February 2010 Keywords: MRSA Infection control Nursing curriculum
s u m m a r y MRSA is becoming more prevalent in healthcare settings and community settings. The purpose of the study is to assess MRSA knowledge among nursing students. A MRSA Survey was administered to nursing students to gauge their general knowledge about MRSA. The scores from the MRSA Survey indicated that nursing students had a knowledge deficit regarding MRSA. Nursing student's need specific MRSA content in the nursing curriculum and need role models in healthcare settings who are following infection control guidelines. A variety of teaching strategies may be used to effectively teach this topic to nursing students. The goal of this education is to prevent the spread of MRSA organisms and decrease the related costs of treating MRSA infections. Published by Elsevier Ltd.
Introduction MRSA (Methicillin-Resistant Staphylococcus aureus) is becoming more prevalent in healthcare settings and MRSA infections have increased over time from accounting for 2% of the total number of staph infections in 1974 to over 63% in 2004 (Centers for Disease Control, 2007). In addition, 18,650 people died during hospitalization related to serious MRSA infections (Centers for Disease Control, 2007). Staphylococcus aureus (MRSA) is a gram positive coccus bacterium that is resistant to certain antibiotics such as oxacillin, penicillin, and amoxicillin. Humans are a natural reservoir of S aureus and 25 to 30% of healthy adults are colonized with MRSA (Centers for Disease Control, 2008). Colonized or infected patients spread MRSA through the contamination of their skin and shedding of organisms into the environment (Oie et al., 2007). Hospital Associated MRSA infections occur most frequently in patients who have weakened immune systems and are manifested as surgical wound infections, urinary tract infections, bloodstream infections, and pneumonia (Centers for Disease Control, 2009). Community-associated (CA) MRSA infections occur in healthy people who have not been recently hospitalized or had a medical procedure (Centers for Disease Control, 2009). Community-associated MRSA infections are commonly manifested as skin infections such as pimples, abscesses, and boils. Hospital Associated MRSA and Community Associated MRSA are both preventable. Educating nursing students about the seriousness of this infection and how to prevent and manage it in the hospitals and communities is an important role for nursing faculty. The goal of this education is to prevent the spread of MRSA organisms and decrease
⁎ Corresponding author. Tel.: + 1 216 791 3800x6032; fax: + 1 216 707 5973. E-mail addresses:
[email protected] (A. Jennings-Sanders),
[email protected] (L. Jury). 0260-6917/$ – see front matter. Published by Elsevier Ltd. doi:10.1016/j.nedt.2010.02.001
the related costs of treating MRSA infections. Thus, the purpose of this study is to assess MRSA knowledge among nursing students. Review of literature A comprehensive review of literature was done using CINAHL and Pub Med search engines. The key words used to do the search included the following: MRSA knowledge, nursing students, and infection control. Limited amount of studies examining MRSA knowledge specifically among nursing students was retrieved. The studies found in the literature addressed general infection control knowledge and hand hygiene practices of nursing students. One such study by Tavolacci et al. (2008) evaluated the knowledge of healthcare students after completion of a module on infection control. Medical students, nursing students, radiologist students, and physiotherapist students taking public health courses were involved in this study. To measure students' knowledge of infection control, multiple choice questions were asked in three areas: standard precautions, hand hygiene, and nosocomial infection. Nursing students had a better mean overall score compared to the other students. Results indicated that the overall score for infection control indicated that the instruction was effective. The best scores were results of tests of standard precautions. Wu et al. (2009) examined preservice Taiwanese nursing students' knowledge, application and confidence with standard and additional precautions in infection control. An Infection Control Evaluation Tool was utilized in this study to determine that the level of knowledge concerning standard and additional precautions was low among Taiwanese nursing students. The authors of the study recommended that the nursing students be required to take a comprehensive foundation course in infection control before entering the clinical environment. Similarly, Celik and Kocasli (2008) explored hygienic hand washing among nursing students. A hand washing questionnaire
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was distributed to 430 nursing students. The study reported that nursing students wash their hands before and after each clinical procedure at a rate of 80% and most of the students (72%) reported that they wash their hands for 1 min or longer. The authors recommended that the education program on hand washing be revised. Lusardi (2007) explored nursing students' experiences of hand decontamination practice in clinical areas by using unstructured interviews and a grounded theory approach. The nine subjects completed their first seven weeks of theory and clinical placements. The four main themes relating to nursing students' perceptions and experiences of hand hygiene in clinical practice included responsibility, influences from peers/staff members, reasons for poor practice, and socialization. The authors concluded that there is a lack of positive influences in the clinical areas for nursing students in terms of hand decontamination. Nursing students in this study decontaminated their hands more often compared to staff. Due to the paucity of literature regarding MRSA knowledge among nursing students, a review of the literature will be discussed regarding MRSA infection control knowledge among healthcare workers in hospital settings. A study that assessed infection control knowledge, attitude, and practice among healthcare workers revealed a good proportion (82%) answered at least 5 of the 11 knowledge statements from a self administered structured questionnaire. Healthcare workers (i.e., nurses and physicians) (n = 392) worked in hospital settings. Response to questions concerning infection control practice illustrated that nurses tended to be better than physicians (p value = 0.204). Both nurses and physicians reported variable compliance to hospital infection control practices in terms of strict adherence. Improvement in infection control training for both groups was recommended by the authors (Ghabrah et al., 2007). Similarly, Paudyal et al. (2008) examined infection control knowledge, attitude, and practice among healthcare workers in a hospital setting. A total of 158 physicians and 166 nurses completed the survey for this study. Results indicated that only 16% and 14% of the respondents achieved maximum scores for knowledge, attitude, and practice items, respectively. Only half of the healthcare workers had heard of methicillin-resistant S. aureus. Logistic regression revealed that profession, age, and studied abroad significantly predicted markers of infection control knowledge, attitudes, and practice. Brady et al. (2008) assessed knowledge of infection control and MRSA guidelines among 52 surgical trainees via a questionnaire. Results indicated that 61.5% of the surgical trainees were misinformed regarding the prevalence of MRSA blood stream infections and 69% were unaware of policies for transfer of MRSA positive patients. Educational training regarding general level of knowledge of infection control was recommended for surgical trainees. In another study conducted by Brady et al. (2009), healthcare workers' knowledge specifically regarding methicillin-resistant S. aureus practice guidelines was examined. Trainee surgeons, members of a non-clinical population, and infection control nurses completed a ten question MRSA practice guideline questionnaire. The mean (SD) score for knowledge for physicians was 6.6 (1.68), nonclinical control population was 4.7 (1.8), and infection control nurses was 8.4 (1.12). Career seniority and gender of the participant were not significant predictors of increased level of knowledge. Easton et al. (2007) assessed infection control and management of MRSA among 174 physicians and 174 nurses by administering a questionnaire. Overall, the findings indicated that many aspects of MRSA and its management were deficient. The authors concluded that assumptions should not be made about adequate knowledge and expertise of staff regarding MRSA. A qualitative study was conducted by Lines (2006) to examine the extent to which staff nurses felt that MRSA was out of control. The semi-structured interviews inquired about the perceptions, attitudes, and beliefs of ten senior staff nurses. Results revealed that 60% of the nurses believed that MRSA was out of control and state “why should they bother worrying about it”. Nurses commented that prescribed
courses of nasal mupirocin were frequently missed and that IV treatments were more important and effective compared to topical agents. The majority of the studies pertaining to knowledge of MRSA among nursing students were descriptive and quantitative in nature. Future studies should have a combination of both quantitative and qualitative methods to extract information that may yield additional insight of why there is a knowledge deficit among nursing students. Larger sample sizes, along with experimental designs could further explain variables associated with MRSA knowledge deficit. Most studies in the review of literature did not have a theoretical framework or model that guided the study when examining MRSA knowledge and infection control measures. Incorporating theoretical frameworks/models (e.g., Theory of Planned Behavior or Health Belief Model) may increase our understanding of variables that may influence behavior relating to infection control measures regarding MRSA.
Methods This pilot study, in which nursing students were asked general questions about their knowledge relating to Methicillin-Resistant Staphylococcus aureus (MRSA), was descriptive in nature. Descriptive research designs describe and document aspects of a particular situation such as MRSA knowledge among nursing students. The study took place during the duration of one semester (approximately 4 months) in the Fall of 2008.This study was approved by the Ethical Institutional Review Board at Cleveland State University in Cleveland, Ohio. Participation or lack of participation in the study would have no impact on the student's grades or progress in the nursing program. Convenience sampling was used by the researcher to efficiently recruit nursing students for this study and to gain immediate insight about MRSA knowledge among nursing students. Sophomore, junior, and senior year nursing students were asked by the researcher to complete a paper version of the MRSA Survey in a classroom setting. After giving written consent, 119 students completed the Demographic Profile and MRSA Survey. The Demographic Profile included questions regarding student status, taking an infection control course/ or in-service, currently doing clinical or working in a hospital, having enough understanding of MRSA, and being satisfied with infection control measures in the healthcare setting. The Methicillin-Resistant Staphylococcus aureus (MRSA) Survey is quantitative in nature. Before utilizing this survey, it was piloted to 10 nursing students who were at various levels in the nursing program. The nursing students gave their feedback about the survey and revisions were done by the authors. The survey asks general knowledge questions regarding MRSA and resistance to antibiotics, how MRSA is spread, the survival time for MRSA, how to reduce your risk of getting MRSA, the potential problems caused by MRSA, and the impact that Chlorine Bleach has on MRSA. The eight questions from the MRSA Survey were based on the content from the Centers for Disease Control and Prevention Guidelines for Environmental Management of MRSA in Community Settings (Centers for Disease Control, 2008). MRSA Survey has not yet been evaluated for test–retest reliability but it has face validity. The questions can reasonably be expected to elicit information regarding the participant's knowledge about MRSA. Prior to their participation in this study, each group of nursing students had exposure to content relating to standard precautions and transmission based precautions. Standard precautions content included hand washing, use of personal protective equipment when handling blood, body substance, excretions, and secretions, prevention of needle stick/sharp injuries, environmental cleaning and spills management, and appropriate handling of waste. Transmission based precaution content included airborne precautions, droplet precautions, and contact precautions. MRSA along with other Hospital Associated infections are discussed in general in each year of the program.
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Analysis of data
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Table 2 One way ANOVA (score on MRSA Survey versus student level).
There were 39 sophomore nursing students, 36 junior nursing students, and 44 senior nursing students. Ninety-five percent of the sophomore, junior, and senior cohorts participated in the study. Fiftythree percent of the nursing students reported taking an infection control course or having an infection control in-service. The majority (96%) of the nursing students were currently doing clinical and/or working in a hospital. Fifty-four percent of the nursing students felt that they did not have enough understanding of MRSA and 52% were not satisfied that all infection control measures were being taken in their current healthcare setting (see Table 1). Based on the eight questions on the MRSA Survey, the total possible mean score is eight. ANOVA and Chi-square analyses were done to analyze the data from the MRSA Survey. A one way ANOVA analysis was performed examining total MRSA Survey scores versus student levels (i.e., sophomore, junior, and senior level students). The mean score for sophomores was 6.25, juniors 6.58, and seniors 6.50. There were no statistically significant differences between the level of students and MRSA Survey scores (F = 0.576) (see Table 2). Chi-square analysis was done to detect statistically significant differences between the correct responses for each question on the MRSA Survey and the level of student (see Table 3). Question #1: MRSA or methicillin-resistant S. aureus is a type of staph that is resistant to certain antibiotics (true statement) (74.3% of the sophomores, 80.5% of the juniors, and 70.4% of the seniors answered this question correctly with a p value of 0.584). Question #2: MRSA infections are usually spread by having contact with someone's skin infection or personal items that they have used like towels, bandages, or razor (true statement) (71.7% of the sophomores, 86.1% of the juniors, and 75.0% of the seniors answered this question correctly with a p value of 0.301). Question #3: Even if surfaces have MRSA on them, this does not mean that you will definitely get an infection if you touch these surfaces(true statement) (87.1% of sophomores, 88.8% juniors, and 90.9% seniors answered this question correctly with a p value of 0.862). Question #4: As with other germs, MRSA can survive on some surfaces for hours, days, and months (true statement) (94.8% of the seniors, 94.4% of the juniors, and 90.9% of the seniors answered this question correctly with a p value of 0.730). Question #5: To reduce your risk of getting MRSA, you should wear gloves and wash your hands with soap (true statement) (58.9% of sophomores, 58.3% juniors, and 68.1% seniors answered this question correctly with a p value of 0.585). Question #6: MRSA is most likely to
Table 1 Demographic profile. Variable
Percentage
Student level Sophomore Junior Senior
33 30 37
Have you ever taken an infection control course/or in-service? Yes No
53 47
Are you currently doing clinical and/or working in a hospital? Yes No
96 4
Do you feel that you have enough understanding of MRSA? Yes No
46 54
Are you satisfied that all infection control measures are being taken in your current healthcare setting? Yes 48 No 52
Sophomores Juniors Seniors F value (0.576)
N
Mean
St. deviation
39 36 44
6.256 6.528 6.500
1.141 1.082 1.455
cause problems when you have a cut or scrap that is covered (false statement) (76.9% of sophomores, 86.1% juniors, and 90.9% seniors answered this question correctly with a p value of 0.201). Question #7: When surfaces are cleaned, MRSA is more likely to survive for longer periods (false statement) (87.1% of sophomores, 83.3% of juniors, and 86.3% of seniors answered this question correctly with a p value of 0.882). Question #8: Chlorine bleach is a broad spectrum disinfectant that can inactivate or kill germs including MRSA (true
Table 3 Chi-square analysis: correct answers for each question versus level of student. Question #1
p value
1. MRSA is a type of staph that is resistant to certain antibodies. (True) Percentage of correct answers Sophomores 74 Juniors 81 Seniors 70
0.584
2. MRSA infections are usually spread by having contact with someone's skin infection or personal items that they have used like towels, bandages, or razor. (True) Percentage of correct answers Sophomores 72 0.301 Juniors 86 Seniors 75 3. Even if surfaces have MRSA on them, this does not mean that you will definitely get an infection if you touch these surfaces. (True) Percentage of correct answers Sophomores 87 0.862 Juniors 89 Seniors 91 4. As with other germs, MRSA can survive on some surfaces for hours, days, and months. (True) Percentage of correct answers Sophomores 95 0.730 Juniors 94 Seniors 91 5. To reduce your risk of getting MRSA, you should wear gloves and wash your hands with soap. (True) Percentage of correct answers Sophomores 59 0.585 Juniors 58 Seniors 68 6. MRSA is most likely to cause problems when you have a cut or scrape that is covered. (False) Percentage of correct answers Sophomores 77 0.201 Juniors 86 Seniors 91 7. When surfaces are cleaned, MRSA is more likely to survive for longer periods. (False) Percentage of correct answers Sophomores 87 0.882 Juniors 83 Seniors 86 8. Chlorine bleach is a broad spectrum disinfectant that can inactivate or kill germs including MRSA. (True) Percentage of correct answers Sophomores 74 0.948 Juniors 75 Seniors 77
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the most efficient teaching strategies for managing cross infections and determining the faculty role by comparing three different teaching methods; scenario-based study groups with and without teacher and simulation training. Findings from the study indicated that scenariobased simulation training made students more aware of how complex each MRSA and Norovirus scenario was. The nursing faculty played an important role in this teaching strategy by asking appropriate questions, giving feedback, and providing hypothetical examples. Nursing faculty should introduce and aid nursing students in their understanding of the guidelines for the prevention of MRSA transmission. This will allow nursing students to become more prepared to participate in evidenced based practice in the prevention of MRSA transmission and other infections. A variety of guidelines are available to assist nursing faculty to better equip nursing students to increase their knowledge about MRSA (see Table 4). Porsha and Richmond (2007) reported that implementation of evidenced based practice protocols for the prevention of MRSA transmission led to an 82% reduction in the rate of MRSA over two years at the Veterans Administration hospital in Pittsburg, Pennsylvania. The authors stressed the importance of having leadership willing to change the culture in the hospital, which will lead to effective promotion of evidence based interventions for the prevention of MRSA transmission. The mean scores from the MRSA tool ranged from 6.25 to 6.50. Overall, these scores indicate that nursing students have some level of understanding about MRSA. However, a more comprehensive infectious disease control program taught across the nursing curriculum would have perhaps increased the scores of the MRSA survey. Chisquare analysis revealed that there were no statistical differences between the correct responses for each question on the MRSA Survey and the level of student. This is yet another indication that all levels of nursing students are getting similar content regarding MRSA. This finding is in contrast to another study conducted by Jenner et al. (2000) where it was found that nursing students' interest in infection control specifically hand washing declines from the first to third year of training. New community-acquired strains of MRSA have affected people who have never been in hospital settings and have none of the identifiable risk factors (Klevens et al., 2007).The literature regarding containment and management of MRSA in community settings is scarce. Nursing students as part of the nursing curriculum have clinical experiences in various community settings such as home care, schools, day care centers, correctional health facilities, occupational health, and community health centers. Therefore, nursing faculty has to educate nursing students on empowering their patients to fight against MRSA infections in community health settings. Students must be aware of
statement) (74.3% of sophomores, 75.0% of juniors, and 77.2% seniors answered this question correctly with a p value of 0.948). Discussion: Implications for nurse educators Results from this pilot study were shared with the undergraduate nursing curriculum committee and recommendations included the following: 1) To assess what specific infection control/MRSA related content is being taught in what courses at all levels in the nursing program. 2) To develop a standard MRSA curriculum that is reinforced at all levels in the nursing program. 3). To develop MRSA educational initiative with nursing education departments in area hospitals where students have clinical experiences in order to further increase understanding of MRSA from a clinical perspective. If other nursing schools are to replicate this study, it is suggested that recommendations be made to curriculum committees to improve student knowledge about MRSA. Students were exposed to general infection control content both in the nursing curriculum and/or in a hospital setting. Despite the exposure to infection control content, more than half of the students felt that they did not have enough understanding of MRSA and were not satisfied that all infection control measures were being taken at their current healthcare setting. This finding suggests that nursing students are expecting more specific content regarding MRSA in the nursing curriculum/hospital in-services and are expressing concern about how the current infection control measures are being practiced in the clinical settings. A study by Lugg and Ahmed (2008) confirmed the above findings in which a self reporting questionnaire that measured adult's and children's nurses knowledge and self reported practices about MRSA was conducted. Results illustrated that the level of knowledge of infection control was inadequate. Adult's nurses scored significantly higher on knowledge and self reported practice than children's nurses. There was no significant difference in either nurse specialty group in self-reported practices between nurses who had received infection control training compared to those who did not receive training. The authors concluded that more educational interventions and training should be implemented for nurses in order to improve knowledge and practice proficiency regarding MRSA. MRSA content can be taught in the form of a case study approach or scenario-based simulation training. Case studies and scenariobased simulation training should include the following content areas regarding MRSA: types of MRSA, transmission of MRSA, signs and symptoms, risk factors for MRSA, prevention with a focus on hand hygiene and barriers to hand hygiene, working with an interdisciplinary team, and treatment of MRSA. Mikkelsen et al. (2008) determined
Table 4 Resources to assist nursing faculty in increasing MRSA knowledge among nursing students. Author
Title
Type
Year
The Society for Healthcare Epidemiology of America
Compendium of strategies to prevent healthcare-associated infections in acute care hospitals Methicillin-Resistant Staphylococcus aureus (MRSA) CDC infection control in healthcare; CA-MRSA: Clinician FAQs Infectious disease, MRSA infection Guidelines for the prevention and management of community associated methicillin-resistant Staphylococcus aureus: A perspective for Canadian healthcare practitioners Evidence-based monitoring strategies and interventions for antibiotic resistant organisms MRSA in healthcare settings
Guidelines (http://www.Shea-online.online.org/about/compendium.cfm)
2008
Fact sheet (http://www.icn.ch/matters_mrsa.htm)
2009
Fact sheet (www.cdcgov/ncidod/dhqp/ar_ca_clinicias.htm#1)
2007
Guide (www.mayoclinic.com/health/mrsa/DS00735) Guide in article Canadian Journal Infectious Disease Medicine Micro-biology, vol 17 Supplemental C September/October
2007 2006
Guide (www.doh.wa.gov/topics/antibiotics/Documents/MRSA-Report-2008pdf).
2008
Guide (http://www.cdc.gov/Features/MRSA)
2007
Guide (http://www.cdc.gov/ncidod/dhqp/ar_mrsa_healthcareFS.html).
2007
International Council of Nurses Centers for Disease Control Mayo Clinic.com Barton et al.
Washington State Department of Health Center for Disease Control and Prevention Center for Disease Control and Prevention
Information about MRSA for healthcare personnel
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the infection prevention measures for MRSA in each setting and be ready to serve as an advocate for their patients. Nursing faculty can work in conjunction with personnel in each community setting to ensure that nursing students are getting reliable and consistent knowledge regarding management of MRSA. Alex and Letizia (2007) report that school nurses must be aware of the risk factors for MRSA and understand its signs, symptoms, diagnostic testing, and management. Student education, early detection, and treatment of MRSA in a school setting are essential in preventing the spread of infection to others in the community. Limitations A greater sample size of students from a multitude of nursing programs would have provided a broader understanding of knowledge that nursing students have about MRSA. Incorporation of pretest and posttest measures would have gauged how much understanding students had after being exposed to MRSA content. Nonetheless, the data from this study provides a starting point for discussion on curricula addressing this content. Conclusion Findings from the study suggest that nursing faculty and nursing education departments in hospitals should provide ongoing education about MRSA to nursing students and nurses. In the clinical setting, if students are caring for patients with MRSA, then nursing faculty must place a special emphasis on the implications of this infection. During clinicals, nursing faculty and experienced nurses must serve as role models to nursing students in terms of adhering to infection control procedures and policies. A variety of teaching strategies may be used to effectively teach this topic to nursing students. There are guidelines to assist nursing faculty to prepare nursing students to have a solid knowledge base of MRSA in order to engage in evidence based practice. Based on the results of this study and future similar studies, personnel working in nursing education departments in hospitals will be able to identify gaps of knowledge that nurses and nursing students may have regarding MRSA. Implementation of in-service training and other teaching strategies to decrease the transmission MRSA pathogens from patient to patient via healthcare providers is essential. Including MRSA content into the nursing curriculum and into inservice programs at hospitals will increase awareness of how to manage Hospital Associated MRSA and Community Associated MRSA. Educating nursing students about MRSA beyond hospital settings is the key. The emergence of Community Associated MRSA infections is
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an additional threat to our society. Both nursing students and nursing faculty must be proactive in educating patients in community settings about MRSA infections to assure positive treatment outcomes. References Alex, A., Letizia, M., 2007. Community-acquired methicillin-resistant Staphylococcus aureus. Considerations for school nurses. The Journal of School Nursing 23 (4), 210–213. Brady, R.R., McDermott, C., Gibb, A.P., Paterson-Brown, S., 2008. Fact or infection: do surgical trainees know enough about infection control? Annals of the Royal College of Surgeons of England 90 (8), 647–650. Brady, R.R., McDermott, C., Cameron, F., Graham, C., Gibb, A.P., 2009. UK healthcare workers' knowledge of methicillin-resistant Staphylococcus aureus practice guidelines: a questionnaire study. Journal of Hospital Infection 73 (3), 264–270. Celik, S., Kocasli, S., 2008. Hygienic hand washing among nursing students in Turkey. Applied Nursing Research 21 (4), 207–211. Centers for Disease Control, 2007. Invasive MRSA. 2007Date Accessed: May 8-2009. http://www.cdc.gov/ncidod/dhqp/ar_mrsa_Invasive_FS.html. Centers for Disease Control, 2008. Community-associated MRSA Information for the Public. 2008Date Accessed: May 6-2009. http://www.cdc.gov/ncidod/dhqp/ar_mrsa_ ca_public.html. Centers for Disease Control, 2009. Community Associated Methicillin Resistant Staphylococcus aureus. 2009Date Accessed: May, 2, 2009. http://www.cdc.gov/ ncidod/dhqp/ar_mrsa_ca.html. Easton, P.M., Sarma, A., Williams, F.L., Marwick, C.A., Phillips, Nathwani, D., 2007. Journal of Hospital Infection 66 (1), 29–33. Ghabrah, T.M., Madani, T.A., Albarrak, A.M., et al., 2007. Assessment of infection control knowledge, attitude and practice among healthcare workers during Hajj period of the Islamic year 1423. Scandinavian Journal of Infectious Diseases 39, 1018–1024. Jenner, E.A., Watson, P.W.B., Miller, L., Boniface, D.R., Jones, F., 2000. A survey of student nurses' attitudes towards hand hygiene practice. Proceedings of the British Psychological Society 9 (1), 68. Klevens, R.M., Morrison, M.A., Nadle, J., et al., 2007. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298, 1763–1771. Lines, L., 2006. A study of senior staff nurses' perceptions about MRSA. Nursing Times 102 (15), 32–35. Lugg, G.R., Ahmed, H.A., 2008. Nurses' perceptions of methicillin-resistant Staphylococcus aureus. British Journal of Infection Control 9 (1), 8–14. Lusardi, G., 2007. Hand hygiene. Nursing Management 14 (6), 26–33. Mikkelsen, J., Reime, M., Harris, A., 2008. Nursing students' learning of managing crossinfections-scenario based simulation training versus study groups. Nurse Education Today 28, 664–671. Oie, S., Suenaga, S., Swa, A., Kamiya, A., 2007. Association between isolation sites of methicillin-resistant Staphylococcus aureus (MRSA) in patients with MRSA-positive body sites and MRSA contamination in their surrounding environmental surfaces. Journal of Infectious Diseases 60, 367–369. Paudyal, P., Simkhada, P., Bruce, J., 2008. Infection control knowledge, attitude, and practice among Nepalese health care workers. American Journal of Infection Control 36 (8), 595–597. Porsha, B., Richmond, I., 2007. Best-practice protocols: reducing harm from MRSA. Nursing Management 38 (8), 22–27. Tavolacci, M.P., Ladner, J., Baily, L., Merle, V., Pitrar, I., Czernichow, P., 2008. Prevention of nosocomial infection and standard precautions: knowledge and source of information among healthcare students. Infection Control Hospital Epidemiology 29 (7), 642–647. Wu, C., Gardner, G.E., Chang, A.M., 2009. Taiwanese nursing students' knowledge, application, and confidence with standard and additional precautions in infection control. Journal of Clinical Nursing 18 (18), 1105–1112.