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Factors associated with personal protection equipment use and hand hygiene among hemodialysis staff
Factors associated with personal protection equipment use and hand hygiene among hemodialysis staff Gayle Shimokura, PhD,a David J. Weber, MD, MPH,a,b William C. Miller, MD, PhD, MPH,a,b Heather Wurtzel, MPH,c and Miriam J. Alter, PhDc Chapel Hill, North Carolina, and Atlanta, Georgia
Background: Because exposure to blood by health care workers is frequent during hemodialysis, gloves are required for all contact with patients and their equipment, followed by hand hygiene. In this study, we investigated factors associated with performing these practices as recommended. Methods: Staff members from a sample of 45 US hemodialysis facilities were surveyed using an anonymous self-administered questionnaire. Factors independently associated with reporting increased compliance with recommended hand hygiene and glove use practices during patient care were identified with multivariate modeling. Results: Of 605 eligible staff members, 420 (69%) responded: registered nurses, 41%; dialysis technicians, 51%; and licensed practical nurses, 8%. Only 35% reported that dialysis patients were at risk for bloodborne virus infections, and only 36% reported always following recommended hand hygiene and glove use practices. Independent factors associated with more frequent compliance were being a technician (versus a registered nurse) and reporting always doing what was needed to protect themselves from infection. Conclusion: Compliance with recommended hand hygiene and glove use practices by hemodialysis staff was low. The rationale for infection control practices specific to the hemodialysis setting was poorly understood by all staff. Infection control training should be tailored to this setting and should address misconceptions. (Am J Infect Control 2006;34:100-7.)
Patient-to-patient transmission of microorganisms via the contaminated hands of health care workers is considered the most important route of transmission of pathogens in health care settings, including hemodialysis facilities.1 Contact transmission can be prevented by hand hygiene (ie, handwashing or use of a waterless hand rub), glove use and removal, and disinfection of environmental surfaces, all of which are elements of Standard Precautions.2-4 Of these, hand hygiene is the most important, because gloves are not required for routine patient care in most health care settings. The use of appropriate hand hygiene has been shown to reduce the rate of infections in inpatient health care settings,5-7 day care centers,8,9 and households.10,11 However, reported rates of adherence to From the Department of Epidemiology, UNC School of Public Health,a and the Department of Medicine, UNC School of Medicine,b Chapel Hill, NC; and the Division of Viral Hepatitis, Centers for Disease Control and Prevention, Atlanta, GA.c Reprint requests: Gayle Shimokura, St. Paul’s Hospital, 1081 Burrard Street, Vancouver BC V6Z 1Y6 Canada. E-mail: [email protected]. Funded by a grant from Glaxo SmithKline. 0196-6553/$32.00 Copyright ª 2006 by the Association for Professionals in Infection Control and Epidemiology, Inc. doi:10.1016/j.ajic.2005.08.012
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handwashing among hospital-based health care workers have been low, averaging 40% (range, 5% to 81 %).3 In the hemodialysis setting, exposure to blood and potentially contaminated fluids can be routinely anticipated; therefore, the use of gloves is required when caring for patients or touching patient equipment.12 Because gloves must be changed between contacts with different patients or after touching potentially contaminated environmental surfaces, the number of times hand hygiene should be performed may be even greater than in the inpatient setting. In a recent study of hand hygiene conducted in hemodialysis facilities, Spanish researchers reported that hands were washed 22% of the time before initiating dialysis, 16% of the time before taking patients off dialysis, and 19% of the time before caring for the blood line.13 Observed and self-reported factors for poor adherence to hand hygiene practices and perceived barriers to appropriate hand hygiene and glove changing policies have been reported (Fig 1).3,14 However, internal motivating factors as barriers, such as staff attitude and knowledge, largely have been unstudied,15 and this continues to be the case among dialysis caregivers. For this reason, we evaluated the role of factors such as perceived risk for hepatitis C virus (HCV) infection and confidence in knowledge of infection control practices in predicting self-reported compliance with hand hygiene and glove changing behaviors.
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Fig 1. Conceptual model of factors influencing adherence to hand hygiene practices.
METHODS Study population A study sample of 53 hemodialysis facilities was selected from all Medicare-approved renal providers in 2000 who served 30 to 150 chronic hemodialysis patients within the continental United States, had been operating for at least 3 years, and were located in cities with at least 4 facilities within a 34-mile radius of one another (to facilitate on-site visits to multiple facilities). The facilities were sampled with equal probability using 2-stage cluster sampling proportional to size. During the period from July 2000 to November 2001, hemodialysis staff members with frequent direct contact with chronic hemodialysis patients from 45 of these participating facilities completed a self-administered anonymous questionnaire. Participants included
registered nurses, licensed practical nurses, and dialysis technicians. Institutional review board approval was obtained from the University of North Carolina at Chapel Hill and the Centers for Disease Control and Prevention. Perception of risk of HCV acquisition, degree of knowledge on how to protect themselves and their patients against bloodborne pathogens, and the frequency with which respondents protected themselves and their patients against bloodborne pathogens were measured using Likert scale items in which respondents chose from 5 possible responses: strongly agree, agree, neutral, disagree, and strongly disagree. Frequency of handwashing and glove use of other staff members at their facility was measured using responses that included: always, often, sometimes, seldom, and never. The practices of other staff members at their facility were used as a surrogate measure of
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Table 1. Self-reported practice of protecting self and patients from bloodborne pathogen transmission, perception of risk for hepatitis C virus infection, and knowledge of infection control among participants, by job category Weighted percentage (95 % CI) of ‘‘strongly agreed’’ response Dialysis technicians (n 5 199)
P
Health care worker always protects (self, patient) from becoming infected with a bloodborne pathogen Self 55.2 (49.7-60.7) 47.0 (34.4-59.5) 65.5 (50.3-80.7) Patient 67.6 (61.9-73.4) 61.8 (52.4-71.3) 75.9 (64.4-87.4)
59.7 70.2
(52.7-66.8) (63.5-76.8)
.01 .03
Perceived at risk group for HCV in hemodialysis setting Health care worker 46.4 (41.4-51.3) Patient 35.0 (29.8-40.2)
(28.7-58.9) (21.5-50.1)
47.8 33.5
(42.0-53.6) (28.0-38.9)
.99 .35
Health care worker knows how to protect (self, patient) from becoming infected with a bloodborne pathogen Self 75.2 (68.9-81.5) 76.3 (69.5-83.1) 83.6 (70.0-97.2) Patient 62.4 (55.2-69.5) 65.8 (56.6-75.1) 70.8 (54.8-86.8)
72.5 57.5
(65.1-80.0) (50.3-64.7)
.28 .18
Total (n 5 415)
Nurses (n 5 181)
45.6 37.6
(36.7-54.5) (28.9-46.2)
LPNs (n 5 35)
43.8 35.8
HCV, hepatitis C virus; LPN, licensed practical nurse.
their own practices because health care workers frequently overestimate their own hand hygiene and glove use. Additional data on patient census at the study facility were obtained from the nursing supervisor or director of the facility. Data on the type of dialysis facility (freestanding or hospital-based) were obtained from a public use database from the Centers for Medicare and Medicaid Services.16
Statistical methods Prevalence estimates, Mantel Haenzel x2 statistics, prevalence ratios, and adjusted and unadjusted prevalence odds ratios and their 95% confidence intervals were calculated, accounting for correlation resulting from the 2-stage cluster sampling design using SUDAAN 8.17 Proportional odds regression modeling was used to identify factors associated with how often staff members reported washing hands and changing gloves before putting patients on dialysis, between going from one station to another, and between administering intravenous medications to different patients using a 3-level ordinal outcome variable. Potential explanatory variables for this model were selected based on prior knowledge and were grouped into 3 categories: demographics (job description and years worked in hemodialysis); potential motivational factors including HCV risk perception, self-reported infection control knowledge, and practice adherence; and other variables (understaffing, frequency of infection control training, and availability of automated sinks). All potential explanatory variables were first evaluated for association with frequency of washing hands and changing gloves using two-way frequency tables, and factors with a statistically significant Mantel Haenzel x2 statistic at the P , .1 level were included in the final model.
RESULTS Of the 605 hemodialysis staff members eligible for participation, 420 (69%) returned questionnaires. Forty-one percent of the respondents were registered nurses, 51% were dialysis technicians, and 8% were licensed practical nurses. They reported an overall median of 5 years of experience working in hemodialysis and 2 years of experience working at the study facility. Overall, 84% of the facilities in which the respondents worked were freestanding centers, a proportion similar to that of all facilities nationwide.
HCV risk perception and confidence in knowledge of infection control practices Most health care workers ‘‘strongly agreed’’ with doing what is needed to protect their patients (68%) and themselves (55%) from becoming infected with a bloodborne pathogen (Table 1). Compared with licensed practical nurses and technicians, registered nurses were significantly less likely to report doing what is needed to protect their patients and themselves. Forty-six percent of respondents ‘‘strongly agreed’’ that they are at risk of becoming infected with HCV by working in hemodialysis. In contrast, only 35% of respondents ‘‘strongly agreed’’ that HCV can be spread from patient-to-patient in the hemodialysis facility. No differences in risk perception by job category were identified. Health care workers also were significantly more likely to report knowing how to protect themselves from becoming infected with a bloodborne pathogen than knowing how to protect their patients (75% versus 62%, P , .01). Infection control training when first hired was reported by almost all respondents (94.5%); however, the frequency of infection control refresher training
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Table 2. Frequency of facility staff handwashing and glove use practices as reported by participants Weighted percentage (95 % CI) Seldom or never (95 % CI)
Sometimes (95 % CI)
No.
Always (95 % CI)
419 419 417
94.8 95.2 42.5
(92.5-97.1) (92.7-97.7) (34.0-51.0)
5.0 4.2 41.8
(2.7-7.3) (1.8-6.7) (35.6-48.1)
0.2 0.6 14.5
(0-0.7) (0-1.2) (10.5-18.5)
0.0 0.0 1.2
(0.1-2.2)
Staff members at dialysis facility wash hands and change gloves. Just before putting patients on dialysis 417 57.4 Between stations 415 46.7 Between administering intravenous medications 409 54.5
(50.2-64.6) (38.7-54.6) (49.1-59.9)
29.7 32.2 26.4
(25.2-34.3) (27.1-37.3) (23.1-29.8)
11.5 17.6 13.4
(6.4-16.6) (13.1-22.0) (9.4-17.3)
1.4 3.6 5.7
(0.2-2.5) (1.9-5.3) (2.8-8.6)
Staff members at dialysis facility wear gloves when. Putting patients on dialysis Taking patients off dialysis Touching equipment or providing patient care
Often (95 % CI)
Table 3. Frequency of facility staff ‘‘always’’ performing handwashing and glove use practices during different activities as reported by participants, by participant’s job category Weighted percentage (95 % CI) of ‘‘always’’ response Total (n 5 415) Staff members at dialysis facility wear gloves when. Putting patients on dialysis Taking patients off dialysis Touching equipment or providing patient care
94.8 95.2 42.5
Staff members at dialysis facility wash hands and change gloves. In between going from one patient care station to another 46.7 In between administering intravenous medications to 54.5 different patients Just before putting patients on dialysis 57.4
Nurses (n 5 181)
LPNs (n 5 35)
Dialysis technicians (n 5 199)
P
(92.5-97.1) (92.7-97.7) (34.0-51.0)
96.4 96.1 33.0
(93.2-99.6) (93.0-99.2) (25.5-40.5)
81.9 81.9 31.3
(62.7-100) (62.5-100) (12.7-49.9)
95.6 96.6 52.4
(92.3-98.9) (93.6-99.6) (40.5-64.3)
.50 .41 .02
(38.8-54.6) (49.1-59.9)
40.8 43.0
(32.0-49.6) (34.0-52.0)
28.3 47.8
(10.0-46.6) (22.5-73.1)
54.0 64.4
(46.0-62.0) (59.3-69.5)
.02 .00
(50.2-64.6)
54.2
(44.9-63.5)
55.9
(35.9-75.9)
59.9
(52.0-67.8)
.46
LPN, licensed practical nurse.
was variable. Among those who had worked at their facility for at least 1 year, most (69.0%) reported that they received infection control refresher training once per year, 18.7% received such training more frequently, and 12.4% received it less often than once per year. When compared by job category, dialysis technicians were significantly less likely to receive at least annual infection control refresher training (84.3%) compared with registered nurses (91.6%) and licensed practical nurses (93.7%) (P 5 .02). Most (80.4%) respondents regardless of job category were completely or somewhat satisfied with the amount of resources available to them to perform their job properly: 33.6% of respondents were completely satisfied, 46.8% were somewhat satisfied, 15.5% were somewhat dissatisfied, and 4.1% were completely dissatisfied. The most common resources they would have liked to see more of were additional staffing (57.9%), staff training (55.0%), and increased space between patient care stations (41.8%).
Handwashing and glove changing practices Ninety-five percent of staff participants reported staff always wearing gloves when putting patients on and taking patients off of dialysis (Table 2). However, only 57% reported staff always washing hands and changing gloves before putting patients on dialysis, 47% between patients care stations, and 55% between patients when administering intravenous medications. Technicians were more likely to report staff handwashing and glove changing for these patient activities than registered nurses and licensed practical nurses (P , .05; Table 3). Responses to handwashing and glove changing practices when moving between patient care stations, between patients to administer intravenous medications, and before initiating a patient’s dialysis were combined into one variable with 3 possible responses: always (ie, both practices, handwashing and glove changing, were always performed in each situation),
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Table 4. Association between demographic characteristics, infection control knowledge and risk perception, and frequency of facility staff handwashing and glove use practices Staff handwashing and glove changing behaviors
Specific characteristic or opinion
No.
Always (95 % CI)
Often or always (95 % CI)
406
35.9
(29.6-42.2)
35.9
(29.9-42.0)
28.2
(21.7-34.7)
189 35 178
43.8 25.6 27.7
(36.5-51.1) (8.0-43.2) (20.7-34.7)
32.2 41.6 40.1
(23.1-41.3) (26.0-57.3) (34.2-46.0)
24.0 32.8 32.2
(16.5-31.5) (13.5-52.0) (23.9-40.4)
.004
1.8 0.9 1.0
(1.3-2.4) (0.4-2.1)
Years worked in hemodialysis ,5.0 years 203 .5.0 years 183
37.3 31.4
(30.1-44.5) (23.9-39.0)
37.5 36.5
(31.0-43.9) (25.5-47.6)
25.2 32.0
(17.4-33.0) (23.0-41.0)
.33
1.3 1.0
(0.9-2.0)
All respondents Demographics Job description Technician LPN Nurse
Often or less often (95 % CI)
Unadjusted prevalence odds ratio (95 % CI)
P
Self-reported practices to prevent infection Health care worker always does what is needed to protect patients from becoming infected with a bloodborne pathogen Strongly agree 248 40.4 (33.3-47.4) 36.4 (29.5-43.2) 23.2 (16.5-30.0) .04 2.0 132 27.2 (19.2-35.3) 33.7 (27.9-39.4) 39.1 (31.8-46.4) 1.0 Othery Health care worker always does what is needed to protect self from becoming infected with a bloodborne pathogen Strongly agree 211 43.4 (35.7-51.0) 35.5 (24.0-47.0) 21.2 (13.6-28.8) .003 4.9 Agree 160 28.5 (19.0-38.0) 39.7 (33.0-46.5) 31.8 (23.8-39.7) 2.7 Othery 35 19.0 (5.1-32.9) 21.4 (8.0-34.7) 59.7 (40.9-78.4) 1.0 HCV risk perception Health care worker is at risk of becoming infected with HCV by working in hemodialysis Strongly agree 184 37.3 (25.6-49.0) 35.7 (26.5-44.8) 27.0 Agree 168 30.5 (19.5-41.4) 38.3 (28.8-47.8) 31.2 Othery 52 43.9 (26.1-61.6) 31.5 (21.3-41.6) 24.7 HCV can be spread from patient-to-patient in the hemodialysis facility Strongly agree 143 37.2 (30.1-44.2) 34.3 (25.8-42.7) Agree 165 35.0 (25.7-44.3) 38.1 (28.2-48.0) Othery 97 34.8 (25.6-44.1) 34.8 (28.1-41.6)
28.6 26.9 30.4
(26.9-41.6) (30.3-45.9)
(1.2-2.4) (0.3-1.7)
(1.3-3.0)
1.4 1.0
(0.8-2.3)
(2.0-11.9) (0.97-7.6)
3.7 2.5 1.0
(1.5-9.2) (0.8-7.5)
.42
0.8 0.6 1.0
(0.3-2.5) (0.3-1.2)
(16.2-40.9) (19.4-34.3) (21.6-39.1)
.79
1.1 1.1 1.0
(0.6-2.1) (0.8-1.5)
.60
1.0 1.0
(0.6-1.6)
0.9 1.0
(0.6-1.2)
Health care worker knows how to protect patients from becoming infected with a bloodborne pathogen Strongly agree 256 34.4 (27.5-41.2) 36.8 (28.4-45.2) 28.8 (21.7-35.9) .70 Othery 148 38.3 (29.7-46.9) 34.7 (28.3-41.0) 27.1 (19.2-34.9) Understaffing Health care worker rates staffing as a high resource priority First or second priority 195 36.9 (28.2-45.6) 34.3 Lower priority 195 34.0 (26.1-41.9) 38.1
1.7 0.8 1.0
(15.0-39.0) (23.3-39.1) (10.3-39.1)
Self-reported level of infection control knowledge Health care worker knows how to protect self from becoming infected with a bloodborne pathogen Strongly agree 308 36.7 (29.3-44.1) 34.2 (26.1-42.3) 29.1 (21.4-36.8) Othery 98 33.5 (22.8-44.1) 41.1 (31.1-51.1) 25.4 (16.6-34.2)
Adjusted prevalence odds ratio* (95 % CI)
28.8 27.9
(22.1-35.6) (19.9-35.8)
.72
1.1 1.0
(0.7-1.5)
Training Frequency that health care worker attends refresher training on infection controld ,1 year 44 43.3 (21.7-64.9) 23.9 (2.6-45.2) 32.8 Once per year 262 32.5 (24.0-41.1) 36.9 (29.5-44.3) 30.6 .1 year 66 33.1 (18.8-47.5) 47.8 (33.1-62.4) 19.1
(23.0-42.6) (25.0-36.2) (9.9-28.3)
.23
0.97 0.80 1.0
(0.4-2.4) (0.5-1.3)
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Table 4. (continued) Staff handwashing and glove changing behaviors
Specific characteristic or opinion
No.
Always (95 % CI)
Often or always (95 % CI)
Availability of automated sinks Facility where health care worker works uses automated sinks No 143 44.2 (35.3-53.2) 31.0 Yes 263 30.3 (22.2-38.3) 39.2
(25.4-36.6) (31.9-46.6)
Often or less often (95 % CI)
24.8 30.5
(13.9-35.6) (23.3-37.7)
P
.03
Unadjusted prevalence odds ratio (95 % CI)
1.6 1.0
(0.9-3.0)
Adjusted prevalence odds ratio* (95 % CI)
1.3 1.0
(0.7-2.6)
HCV, hepatitis C virus; LPN, licensed practical nurse. *Model included only those variables with reported odds ratios. The odds ratios measure the odds from the ‘‘always’’ category to ‘‘always or often’’ category, and the odds from the ‘‘always or often’’ category to the ‘‘often or less often’’ category. y ‘‘Agree’’ and ‘‘other’’ categories were combined when the ‘‘other’’ category would otherwise have had ,30 responses. d Analysis was limited to participants who had an opportunity to have annual training. In other words, participants who had been employed at the study facility for less than 1 year and had not yet received any training were excluded from this analysis (n 5 27).
often (ie, at least one practice was often but not always performed in each situation), and not often (ie, at least one practice was not often performed in each situation) (Table 4). Using this combined variable as a measure of adherence, the proportion of all respondents that reported staff always performing handwashing and changing gloves decreased to 36%; 44% among technicians, 28% among registered nurses, and 26% among licensed practical nurses (Table 4). The responses to this combined variable were also used as measures of compliance to determine which of the factors evaluated in the survey were associated with increased adherence to recommended hand hygiene and glove changing practices. In the unadjusted analysis, 4 factors were found to be associated with increased adherence to hand hygiene and glove changing practices: job category (ie, dialysis technician), always doing what is needed to protect patients from becoming infected with a bloodborne pathogen, always doing what is needed to protect self from becoming infected with a bloodborne pathogen, and working in a facility that does not use automated sinks (Table 4). Of these, being a dialysis technician and always doing what is needed to protect self from becoming infected with a bloodborne pathogen were identified as independent factors associated with increased compliance after simultaneous adjustment for other factors (Table 4).
DISCUSSION Hepatitis C is the most frequent disease leading to liver transplantation in the United States. Serologic surveys of hemodialysis patients have consistently shown higher prevalence estimates than in the general public.18,19 The higher prevalence estimates of both HCV and hepatitis B virus infection and the results of outbreak investigations suggest that HCV (and hepatitis B
virus) transmission occurs within hemodialysis centers as a result of inadequate infection control practices. For this reason, we studied factors associated with hand hygiene and glove use among hemodialysis staff. Standard precautions are recommended by the Centers for Disease Control and Prevention when caring for all patients and include hand hygiene before and after patient contact and wearing gloves for procedures that are likely to involve contact with blood or contaminated body fluids. Studies have generally documented poor compliance with these practices, particularly with hand hygiene.3 In one recent study of hospitalbased health care workers, two-thirds reported routinely wearing gloves when performing an invasive procedure, but less than half reported washing their hands after patient care20; a similar study among European hemodialysis staff also reported this tendency for staff to use gloves but not to wash hands.13 In the hemodialysis setting, handwashing and glove changing are required more often because exposure to blood and potentially contaminated items can be routinely anticipated. Thus, gloves are required whenever caring for a patient or touching the patient’s equipment. In addition, any item at the patient’s dialysis station is considered potentially contaminated. Therefore, gloves must be removed after leaving each patient’s station and a new pair donned before entering another patient’s station, even from a clean area. Frequent glove use requires frequent hand hygiene. Hand hygiene should always be performed after gloves are removed and between patient contacts, as well as after touching blood, body fluids, and contaminated items. Our study is the first to evaluate compliance with these recommendations among hemodialysis staff in the United States. We measured individual compliance by asking participants to assess the frequency of
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handwashing and glove use of staff members at the facility. We thought that use of this surrogate marker was needed because self-assessment of behavior often results in a bias toward the socially desirable behavior, and that reporting others’ compliance would provide a more accurate reflection of their own compliance. Using this methodology, we found that only about one-third of subjects reported always following the recommended hand hygiene and glove changing practices. Importantly, registered nurses were significantly less likely to follow these practices than were dialysis technicians. This study also showed that health care workers who reported frequent compliance with hand hygiene and glove changing were more likely to place a high value on protecting themselves from bloodborne infections. These associations were not affected by levels of HCV risk perception, differences in knowledge on how to protect themselves and their patients from bloodborne pathogen infections, frequency of infection control refresher training, or perceived need for more staff at the facility. In our study, the strongest predictor of following recommended hand hygiene and glove use practices was the workers’ belief they were doing what was needed to protect themselves from becoming infected with a bloodborne pathogen. Because most studies of factors associated with health care workers’ hand hygiene practices did not differentiate between practices designed to protect patients from those that protect the worker, it is difficult to compare our results with those of previous studies. O’Boyle et al reported that hand hygiene behavior may be more sensitive to the intensity of work activity in the clinical setting than to internal motivational factors, with lower adherence when the nursing unit was busier.15 The finding that dialysis technicians as a category were independently associated with increased adherence to the recommendations suggests that there are unmeasured differences between technicians and registered nurses that need to be further elucidated. There are both real and perceived barriers to improving hand hygiene and glove use practices among hemodialysis staff, including higher patient-to-staff ratios and lack of understanding of the need for such practices. Although this study did not address what measures might be effective in improving practices, the results suggest that interventions should focus on the level of infection control knowledge and frequency of infection control training. The results also suggest that staff with professional licenses are not necessarily knowledgeable about appropriate infection control practices or that they follow them; thus, initial and continuing education programs need to target this group regarding infection control practices specific to hemodialysis settings. Ensuring that staffing levels are
sufficient to support adequate infection control practices, particularly during patient turnover, and increasing the availability of waterless hand rubs (see Fig. 1) may also increase compliance with recommended hand hygiene and glove changing practices in the hemodialysis setting. Future studies should focus on evaluating specific interventions to increase compliance with recommended infection control practices in this caregiver population. The authors acknowledge the contributions of the dialysis staff who participated in the survey, as well as the tireless efforts of our research staff who collected the data, Allys Anselmi, Mary Kirkland, Suzanne Moore, Alice White, and Teresa Womack, as well as statistical advice from Gregory P. Samsa, PhD, and general support from William A. Rutala, PhD, MPH.
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18. Finelli L, Miller JT, Tokars JT, Alter MJ, Arduino MJ. National surveillance of dialysis-associated diseases in the United States, 2002. Semin Dial 2005;18:52-61. 19. Alter MJ. Hepatitis C virus infection in the United States. J Hepatol 1999;31(Suppl 1):88-91. 20. Doebbeling BN, Vaughn TE, McCoy KD, Beekmann SE, Woolson RF, Ferguson KJ, et al. Percutaneous injury, blood exposure, and adherence to standard precautions: are hospital-based health care providers still at risk? Clin Infect Dis 2003;37:1006-13.
Background: Because exposure to blood by health care workers is frequent during hemodialysis, gloves are required for all contact with patients and their equipment, followed by hand hygiene. In this study, we investigated factors associated with performing these practices as recommended. Methods: Staff members from a sample of 45 US hemodialysis facilities were surveyed using an anonymous self-administered questionnaire. Factors independently associated with reporting increased compliance with recommended hand hygiene and glove use practices during patient care were identified with multivariate modeling. Results: Of 605 eligible staff members, 420 (69%) responded: registered nurses, 41%; dialysis technicians, 51%; and licensed practical nurses, 8%. Only 35% reported that dialysis patients were at risk for bloodborne virus infections, and only 36% reported always following recommended hand hygiene and glove use practices. Independent factors associated with more frequent compliance were being a technician (versus a registered nurse) and reporting always doing what was needed to protect themselves from infection. Conclusion: Compliance with recommended hand hygiene and glove use practices by hemodialysis staff was low. The rationale for infection control practices specific to the hemodialysis setting was poorly understood by all staff. Infection control training should be tailored to this setting and should address misconceptions. (Am J Infect Control 2006;34:100-7.)
Patient-to-patient transmission of microorganisms via the contaminated hands of health care workers is considered the most important route of transmission of pathogens in health care settings, including hemodialysis facilities.1 Contact transmission can be prevented by hand hygiene (ie, handwashing or use of a waterless hand rub), glove use and removal, and disinfection of environmental surfaces, all of which are elements of Standard Precautions.2-4 Of these, hand hygiene is the most important, because gloves are not required for routine patient care in most health care settings. The use of appropriate hand hygiene has been shown to reduce the rate of infections in inpatient health care settings,5-7 day care centers,8,9 and households.10,11 However, reported rates of adherence to From the Department of Epidemiology, UNC School of Public Health,a and the Department of Medicine, UNC School of Medicine,b Chapel Hill, NC; and the Division of Viral Hepatitis, Centers for Disease Control and Prevention, Atlanta, GA.c Reprint requests: Gayle Shimokura, St. Paul’s Hospital, 1081 Burrard Street, Vancouver BC V6Z 1Y6 Canada. E-mail: [email protected]. Funded by a grant from Glaxo SmithKline. 0196-6553/$32.00 Copyright ª 2006 by the Association for Professionals in Infection Control and Epidemiology, Inc. doi:10.1016/j.ajic.2005.08.012
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handwashing among hospital-based health care workers have been low, averaging 40% (range, 5% to 81 %).3 In the hemodialysis setting, exposure to blood and potentially contaminated fluids can be routinely anticipated; therefore, the use of gloves is required when caring for patients or touching patient equipment.12 Because gloves must be changed between contacts with different patients or after touching potentially contaminated environmental surfaces, the number of times hand hygiene should be performed may be even greater than in the inpatient setting. In a recent study of hand hygiene conducted in hemodialysis facilities, Spanish researchers reported that hands were washed 22% of the time before initiating dialysis, 16% of the time before taking patients off dialysis, and 19% of the time before caring for the blood line.13 Observed and self-reported factors for poor adherence to hand hygiene practices and perceived barriers to appropriate hand hygiene and glove changing policies have been reported (Fig 1).3,14 However, internal motivating factors as barriers, such as staff attitude and knowledge, largely have been unstudied,15 and this continues to be the case among dialysis caregivers. For this reason, we evaluated the role of factors such as perceived risk for hepatitis C virus (HCV) infection and confidence in knowledge of infection control practices in predicting self-reported compliance with hand hygiene and glove changing behaviors.
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Fig 1. Conceptual model of factors influencing adherence to hand hygiene practices.
METHODS Study population A study sample of 53 hemodialysis facilities was selected from all Medicare-approved renal providers in 2000 who served 30 to 150 chronic hemodialysis patients within the continental United States, had been operating for at least 3 years, and were located in cities with at least 4 facilities within a 34-mile radius of one another (to facilitate on-site visits to multiple facilities). The facilities were sampled with equal probability using 2-stage cluster sampling proportional to size. During the period from July 2000 to November 2001, hemodialysis staff members with frequent direct contact with chronic hemodialysis patients from 45 of these participating facilities completed a self-administered anonymous questionnaire. Participants included
registered nurses, licensed practical nurses, and dialysis technicians. Institutional review board approval was obtained from the University of North Carolina at Chapel Hill and the Centers for Disease Control and Prevention. Perception of risk of HCV acquisition, degree of knowledge on how to protect themselves and their patients against bloodborne pathogens, and the frequency with which respondents protected themselves and their patients against bloodborne pathogens were measured using Likert scale items in which respondents chose from 5 possible responses: strongly agree, agree, neutral, disagree, and strongly disagree. Frequency of handwashing and glove use of other staff members at their facility was measured using responses that included: always, often, sometimes, seldom, and never. The practices of other staff members at their facility were used as a surrogate measure of
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Table 1. Self-reported practice of protecting self and patients from bloodborne pathogen transmission, perception of risk for hepatitis C virus infection, and knowledge of infection control among participants, by job category Weighted percentage (95 % CI) of ‘‘strongly agreed’’ response Dialysis technicians (n 5 199)
P
Health care worker always protects (self, patient) from becoming infected with a bloodborne pathogen Self 55.2 (49.7-60.7) 47.0 (34.4-59.5) 65.5 (50.3-80.7) Patient 67.6 (61.9-73.4) 61.8 (52.4-71.3) 75.9 (64.4-87.4)
59.7 70.2
(52.7-66.8) (63.5-76.8)
.01 .03
Perceived at risk group for HCV in hemodialysis setting Health care worker 46.4 (41.4-51.3) Patient 35.0 (29.8-40.2)
(28.7-58.9) (21.5-50.1)
47.8 33.5
(42.0-53.6) (28.0-38.9)
.99 .35
Health care worker knows how to protect (self, patient) from becoming infected with a bloodborne pathogen Self 75.2 (68.9-81.5) 76.3 (69.5-83.1) 83.6 (70.0-97.2) Patient 62.4 (55.2-69.5) 65.8 (56.6-75.1) 70.8 (54.8-86.8)
72.5 57.5
(65.1-80.0) (50.3-64.7)
.28 .18
Total (n 5 415)
Nurses (n 5 181)
45.6 37.6
(36.7-54.5) (28.9-46.2)
LPNs (n 5 35)
43.8 35.8
HCV, hepatitis C virus; LPN, licensed practical nurse.
their own practices because health care workers frequently overestimate their own hand hygiene and glove use. Additional data on patient census at the study facility were obtained from the nursing supervisor or director of the facility. Data on the type of dialysis facility (freestanding or hospital-based) were obtained from a public use database from the Centers for Medicare and Medicaid Services.16
Statistical methods Prevalence estimates, Mantel Haenzel x2 statistics, prevalence ratios, and adjusted and unadjusted prevalence odds ratios and their 95% confidence intervals were calculated, accounting for correlation resulting from the 2-stage cluster sampling design using SUDAAN 8.17 Proportional odds regression modeling was used to identify factors associated with how often staff members reported washing hands and changing gloves before putting patients on dialysis, between going from one station to another, and between administering intravenous medications to different patients using a 3-level ordinal outcome variable. Potential explanatory variables for this model were selected based on prior knowledge and were grouped into 3 categories: demographics (job description and years worked in hemodialysis); potential motivational factors including HCV risk perception, self-reported infection control knowledge, and practice adherence; and other variables (understaffing, frequency of infection control training, and availability of automated sinks). All potential explanatory variables were first evaluated for association with frequency of washing hands and changing gloves using two-way frequency tables, and factors with a statistically significant Mantel Haenzel x2 statistic at the P , .1 level were included in the final model.
RESULTS Of the 605 hemodialysis staff members eligible for participation, 420 (69%) returned questionnaires. Forty-one percent of the respondents were registered nurses, 51% were dialysis technicians, and 8% were licensed practical nurses. They reported an overall median of 5 years of experience working in hemodialysis and 2 years of experience working at the study facility. Overall, 84% of the facilities in which the respondents worked were freestanding centers, a proportion similar to that of all facilities nationwide.
HCV risk perception and confidence in knowledge of infection control practices Most health care workers ‘‘strongly agreed’’ with doing what is needed to protect their patients (68%) and themselves (55%) from becoming infected with a bloodborne pathogen (Table 1). Compared with licensed practical nurses and technicians, registered nurses were significantly less likely to report doing what is needed to protect their patients and themselves. Forty-six percent of respondents ‘‘strongly agreed’’ that they are at risk of becoming infected with HCV by working in hemodialysis. In contrast, only 35% of respondents ‘‘strongly agreed’’ that HCV can be spread from patient-to-patient in the hemodialysis facility. No differences in risk perception by job category were identified. Health care workers also were significantly more likely to report knowing how to protect themselves from becoming infected with a bloodborne pathogen than knowing how to protect their patients (75% versus 62%, P , .01). Infection control training when first hired was reported by almost all respondents (94.5%); however, the frequency of infection control refresher training
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Table 2. Frequency of facility staff handwashing and glove use practices as reported by participants Weighted percentage (95 % CI) Seldom or never (95 % CI)
Sometimes (95 % CI)
No.
Always (95 % CI)
419 419 417
94.8 95.2 42.5
(92.5-97.1) (92.7-97.7) (34.0-51.0)
5.0 4.2 41.8
(2.7-7.3) (1.8-6.7) (35.6-48.1)
0.2 0.6 14.5
(0-0.7) (0-1.2) (10.5-18.5)
0.0 0.0 1.2
(0.1-2.2)
Staff members at dialysis facility wash hands and change gloves. Just before putting patients on dialysis 417 57.4 Between stations 415 46.7 Between administering intravenous medications 409 54.5
(50.2-64.6) (38.7-54.6) (49.1-59.9)
29.7 32.2 26.4
(25.2-34.3) (27.1-37.3) (23.1-29.8)
11.5 17.6 13.4
(6.4-16.6) (13.1-22.0) (9.4-17.3)
1.4 3.6 5.7
(0.2-2.5) (1.9-5.3) (2.8-8.6)
Staff members at dialysis facility wear gloves when. Putting patients on dialysis Taking patients off dialysis Touching equipment or providing patient care
Often (95 % CI)
Table 3. Frequency of facility staff ‘‘always’’ performing handwashing and glove use practices during different activities as reported by participants, by participant’s job category Weighted percentage (95 % CI) of ‘‘always’’ response Total (n 5 415) Staff members at dialysis facility wear gloves when. Putting patients on dialysis Taking patients off dialysis Touching equipment or providing patient care
94.8 95.2 42.5
Staff members at dialysis facility wash hands and change gloves. In between going from one patient care station to another 46.7 In between administering intravenous medications to 54.5 different patients Just before putting patients on dialysis 57.4
Nurses (n 5 181)
LPNs (n 5 35)
Dialysis technicians (n 5 199)
P
(92.5-97.1) (92.7-97.7) (34.0-51.0)
96.4 96.1 33.0
(93.2-99.6) (93.0-99.2) (25.5-40.5)
81.9 81.9 31.3
(62.7-100) (62.5-100) (12.7-49.9)
95.6 96.6 52.4
(92.3-98.9) (93.6-99.6) (40.5-64.3)
.50 .41 .02
(38.8-54.6) (49.1-59.9)
40.8 43.0
(32.0-49.6) (34.0-52.0)
28.3 47.8
(10.0-46.6) (22.5-73.1)
54.0 64.4
(46.0-62.0) (59.3-69.5)
.02 .00
(50.2-64.6)
54.2
(44.9-63.5)
55.9
(35.9-75.9)
59.9
(52.0-67.8)
.46
LPN, licensed practical nurse.
was variable. Among those who had worked at their facility for at least 1 year, most (69.0%) reported that they received infection control refresher training once per year, 18.7% received such training more frequently, and 12.4% received it less often than once per year. When compared by job category, dialysis technicians were significantly less likely to receive at least annual infection control refresher training (84.3%) compared with registered nurses (91.6%) and licensed practical nurses (93.7%) (P 5 .02). Most (80.4%) respondents regardless of job category were completely or somewhat satisfied with the amount of resources available to them to perform their job properly: 33.6% of respondents were completely satisfied, 46.8% were somewhat satisfied, 15.5% were somewhat dissatisfied, and 4.1% were completely dissatisfied. The most common resources they would have liked to see more of were additional staffing (57.9%), staff training (55.0%), and increased space between patient care stations (41.8%).
Handwashing and glove changing practices Ninety-five percent of staff participants reported staff always wearing gloves when putting patients on and taking patients off of dialysis (Table 2). However, only 57% reported staff always washing hands and changing gloves before putting patients on dialysis, 47% between patients care stations, and 55% between patients when administering intravenous medications. Technicians were more likely to report staff handwashing and glove changing for these patient activities than registered nurses and licensed practical nurses (P , .05; Table 3). Responses to handwashing and glove changing practices when moving between patient care stations, between patients to administer intravenous medications, and before initiating a patient’s dialysis were combined into one variable with 3 possible responses: always (ie, both practices, handwashing and glove changing, were always performed in each situation),
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Table 4. Association between demographic characteristics, infection control knowledge and risk perception, and frequency of facility staff handwashing and glove use practices Staff handwashing and glove changing behaviors
Specific characteristic or opinion
No.
Always (95 % CI)
Often or always (95 % CI)
406
35.9
(29.6-42.2)
35.9
(29.9-42.0)
28.2
(21.7-34.7)
189 35 178
43.8 25.6 27.7
(36.5-51.1) (8.0-43.2) (20.7-34.7)
32.2 41.6 40.1
(23.1-41.3) (26.0-57.3) (34.2-46.0)
24.0 32.8 32.2
(16.5-31.5) (13.5-52.0) (23.9-40.4)
.004
1.8 0.9 1.0
(1.3-2.4) (0.4-2.1)
Years worked in hemodialysis ,5.0 years 203 .5.0 years 183
37.3 31.4
(30.1-44.5) (23.9-39.0)
37.5 36.5
(31.0-43.9) (25.5-47.6)
25.2 32.0
(17.4-33.0) (23.0-41.0)
.33
1.3 1.0
(0.9-2.0)
All respondents Demographics Job description Technician LPN Nurse
Often or less often (95 % CI)
Unadjusted prevalence odds ratio (95 % CI)
P
Self-reported practices to prevent infection Health care worker always does what is needed to protect patients from becoming infected with a bloodborne pathogen Strongly agree 248 40.4 (33.3-47.4) 36.4 (29.5-43.2) 23.2 (16.5-30.0) .04 2.0 132 27.2 (19.2-35.3) 33.7 (27.9-39.4) 39.1 (31.8-46.4) 1.0 Othery Health care worker always does what is needed to protect self from becoming infected with a bloodborne pathogen Strongly agree 211 43.4 (35.7-51.0) 35.5 (24.0-47.0) 21.2 (13.6-28.8) .003 4.9 Agree 160 28.5 (19.0-38.0) 39.7 (33.0-46.5) 31.8 (23.8-39.7) 2.7 Othery 35 19.0 (5.1-32.9) 21.4 (8.0-34.7) 59.7 (40.9-78.4) 1.0 HCV risk perception Health care worker is at risk of becoming infected with HCV by working in hemodialysis Strongly agree 184 37.3 (25.6-49.0) 35.7 (26.5-44.8) 27.0 Agree 168 30.5 (19.5-41.4) 38.3 (28.8-47.8) 31.2 Othery 52 43.9 (26.1-61.6) 31.5 (21.3-41.6) 24.7 HCV can be spread from patient-to-patient in the hemodialysis facility Strongly agree 143 37.2 (30.1-44.2) 34.3 (25.8-42.7) Agree 165 35.0 (25.7-44.3) 38.1 (28.2-48.0) Othery 97 34.8 (25.6-44.1) 34.8 (28.1-41.6)
28.6 26.9 30.4
(26.9-41.6) (30.3-45.9)
(1.2-2.4) (0.3-1.7)
(1.3-3.0)
1.4 1.0
(0.8-2.3)
(2.0-11.9) (0.97-7.6)
3.7 2.5 1.0
(1.5-9.2) (0.8-7.5)
.42
0.8 0.6 1.0
(0.3-2.5) (0.3-1.2)
(16.2-40.9) (19.4-34.3) (21.6-39.1)
.79
1.1 1.1 1.0
(0.6-2.1) (0.8-1.5)
.60
1.0 1.0
(0.6-1.6)
0.9 1.0
(0.6-1.2)
Health care worker knows how to protect patients from becoming infected with a bloodborne pathogen Strongly agree 256 34.4 (27.5-41.2) 36.8 (28.4-45.2) 28.8 (21.7-35.9) .70 Othery 148 38.3 (29.7-46.9) 34.7 (28.3-41.0) 27.1 (19.2-34.9) Understaffing Health care worker rates staffing as a high resource priority First or second priority 195 36.9 (28.2-45.6) 34.3 Lower priority 195 34.0 (26.1-41.9) 38.1
1.7 0.8 1.0
(15.0-39.0) (23.3-39.1) (10.3-39.1)
Self-reported level of infection control knowledge Health care worker knows how to protect self from becoming infected with a bloodborne pathogen Strongly agree 308 36.7 (29.3-44.1) 34.2 (26.1-42.3) 29.1 (21.4-36.8) Othery 98 33.5 (22.8-44.1) 41.1 (31.1-51.1) 25.4 (16.6-34.2)
Adjusted prevalence odds ratio* (95 % CI)
28.8 27.9
(22.1-35.6) (19.9-35.8)
.72
1.1 1.0
(0.7-1.5)
Training Frequency that health care worker attends refresher training on infection controld ,1 year 44 43.3 (21.7-64.9) 23.9 (2.6-45.2) 32.8 Once per year 262 32.5 (24.0-41.1) 36.9 (29.5-44.3) 30.6 .1 year 66 33.1 (18.8-47.5) 47.8 (33.1-62.4) 19.1
(23.0-42.6) (25.0-36.2) (9.9-28.3)
.23
0.97 0.80 1.0
(0.4-2.4) (0.5-1.3)
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Table 4. (continued) Staff handwashing and glove changing behaviors
Specific characteristic or opinion
No.
Always (95 % CI)
Often or always (95 % CI)
Availability of automated sinks Facility where health care worker works uses automated sinks No 143 44.2 (35.3-53.2) 31.0 Yes 263 30.3 (22.2-38.3) 39.2
(25.4-36.6) (31.9-46.6)
Often or less often (95 % CI)
24.8 30.5
(13.9-35.6) (23.3-37.7)
P
.03
Unadjusted prevalence odds ratio (95 % CI)
1.6 1.0
(0.9-3.0)
Adjusted prevalence odds ratio* (95 % CI)
1.3 1.0
(0.7-2.6)
HCV, hepatitis C virus; LPN, licensed practical nurse. *Model included only those variables with reported odds ratios. The odds ratios measure the odds from the ‘‘always’’ category to ‘‘always or often’’ category, and the odds from the ‘‘always or often’’ category to the ‘‘often or less often’’ category. y ‘‘Agree’’ and ‘‘other’’ categories were combined when the ‘‘other’’ category would otherwise have had ,30 responses. d Analysis was limited to participants who had an opportunity to have annual training. In other words, participants who had been employed at the study facility for less than 1 year and had not yet received any training were excluded from this analysis (n 5 27).
often (ie, at least one practice was often but not always performed in each situation), and not often (ie, at least one practice was not often performed in each situation) (Table 4). Using this combined variable as a measure of adherence, the proportion of all respondents that reported staff always performing handwashing and changing gloves decreased to 36%; 44% among technicians, 28% among registered nurses, and 26% among licensed practical nurses (Table 4). The responses to this combined variable were also used as measures of compliance to determine which of the factors evaluated in the survey were associated with increased adherence to recommended hand hygiene and glove changing practices. In the unadjusted analysis, 4 factors were found to be associated with increased adherence to hand hygiene and glove changing practices: job category (ie, dialysis technician), always doing what is needed to protect patients from becoming infected with a bloodborne pathogen, always doing what is needed to protect self from becoming infected with a bloodborne pathogen, and working in a facility that does not use automated sinks (Table 4). Of these, being a dialysis technician and always doing what is needed to protect self from becoming infected with a bloodborne pathogen were identified as independent factors associated with increased compliance after simultaneous adjustment for other factors (Table 4).
DISCUSSION Hepatitis C is the most frequent disease leading to liver transplantation in the United States. Serologic surveys of hemodialysis patients have consistently shown higher prevalence estimates than in the general public.18,19 The higher prevalence estimates of both HCV and hepatitis B virus infection and the results of outbreak investigations suggest that HCV (and hepatitis B
virus) transmission occurs within hemodialysis centers as a result of inadequate infection control practices. For this reason, we studied factors associated with hand hygiene and glove use among hemodialysis staff. Standard precautions are recommended by the Centers for Disease Control and Prevention when caring for all patients and include hand hygiene before and after patient contact and wearing gloves for procedures that are likely to involve contact with blood or contaminated body fluids. Studies have generally documented poor compliance with these practices, particularly with hand hygiene.3 In one recent study of hospitalbased health care workers, two-thirds reported routinely wearing gloves when performing an invasive procedure, but less than half reported washing their hands after patient care20; a similar study among European hemodialysis staff also reported this tendency for staff to use gloves but not to wash hands.13 In the hemodialysis setting, handwashing and glove changing are required more often because exposure to blood and potentially contaminated items can be routinely anticipated. Thus, gloves are required whenever caring for a patient or touching the patient’s equipment. In addition, any item at the patient’s dialysis station is considered potentially contaminated. Therefore, gloves must be removed after leaving each patient’s station and a new pair donned before entering another patient’s station, even from a clean area. Frequent glove use requires frequent hand hygiene. Hand hygiene should always be performed after gloves are removed and between patient contacts, as well as after touching blood, body fluids, and contaminated items. Our study is the first to evaluate compliance with these recommendations among hemodialysis staff in the United States. We measured individual compliance by asking participants to assess the frequency of
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handwashing and glove use of staff members at the facility. We thought that use of this surrogate marker was needed because self-assessment of behavior often results in a bias toward the socially desirable behavior, and that reporting others’ compliance would provide a more accurate reflection of their own compliance. Using this methodology, we found that only about one-third of subjects reported always following the recommended hand hygiene and glove changing practices. Importantly, registered nurses were significantly less likely to follow these practices than were dialysis technicians. This study also showed that health care workers who reported frequent compliance with hand hygiene and glove changing were more likely to place a high value on protecting themselves from bloodborne infections. These associations were not affected by levels of HCV risk perception, differences in knowledge on how to protect themselves and their patients from bloodborne pathogen infections, frequency of infection control refresher training, or perceived need for more staff at the facility. In our study, the strongest predictor of following recommended hand hygiene and glove use practices was the workers’ belief they were doing what was needed to protect themselves from becoming infected with a bloodborne pathogen. Because most studies of factors associated with health care workers’ hand hygiene practices did not differentiate between practices designed to protect patients from those that protect the worker, it is difficult to compare our results with those of previous studies. O’Boyle et al reported that hand hygiene behavior may be more sensitive to the intensity of work activity in the clinical setting than to internal motivational factors, with lower adherence when the nursing unit was busier.15 The finding that dialysis technicians as a category were independently associated with increased adherence to the recommendations suggests that there are unmeasured differences between technicians and registered nurses that need to be further elucidated. There are both real and perceived barriers to improving hand hygiene and glove use practices among hemodialysis staff, including higher patient-to-staff ratios and lack of understanding of the need for such practices. Although this study did not address what measures might be effective in improving practices, the results suggest that interventions should focus on the level of infection control knowledge and frequency of infection control training. The results also suggest that staff with professional licenses are not necessarily knowledgeable about appropriate infection control practices or that they follow them; thus, initial and continuing education programs need to target this group regarding infection control practices specific to hemodialysis settings. Ensuring that staffing levels are
sufficient to support adequate infection control practices, particularly during patient turnover, and increasing the availability of waterless hand rubs (see Fig. 1) may also increase compliance with recommended hand hygiene and glove changing practices in the hemodialysis setting. Future studies should focus on evaluating specific interventions to increase compliance with recommended infection control practices in this caregiver population. The authors acknowledge the contributions of the dialysis staff who participated in the survey, as well as the tireless efforts of our research staff who collected the data, Allys Anselmi, Mary Kirkland, Suzanne Moore, Alice White, and Teresa Womack, as well as statistical advice from Gregory P. Samsa, PhD, and general support from William A. Rutala, PhD, MPH.
References 1. Centers for Disease Control and Prevention. Recommendations for preventing transmission of infections among chronic hemodialysis patients. MMWR 2001;50(No. RR-5):1-43. 2. Garner JS. Guideline for isolation precautions in hospitals. The Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol 1996;17:53-80. 3. The Healthcare Infection Control Practices Advisory Committee, HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Guideline for hand hygiene in health-care settings: Recommendations of the Healthcare Infection Control Advisory Committee and the HICPAC/ SHEA/APIC/IDSA Hand Hygiene Task Force. MMWR 2002;51 (No. RR-16):1-48. 4. Centers for Disease Control and Prevention. Guidelines for environmental infection control in health-care facilities: recommendations of CDC and the Healthcare Infection Control Practices Advisory Committee (HICPAC). MMWR 2003;52(No. RR-10):1-48. 5. Daniels IR. Historical perspectives on health. Semmelweis: a lesson to relearn? J R Soc Health 1998;118:367-70. 6. Larson EL, Early E, Cloonan P, Sugrue S, Parides M. An organizational climate intervention associated with increased handwashing and decreased nosocomial infections. Behavioral Med 2000;26: 14-22. 7. Pittet D, Hugonnet S, Harbarth S, Mourouga P, Sauvan V, Touveneau S, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 2000;356:1307-12. 8. Niffenegger JP. Proper handwashing promotes wellness in child care. J Pediatr Health Care 1997;11:26-31. 9. Roberts L, Jorm L, Patel M, Smith W, Douglas RM, McGilchrist C. Effect of infection control measures on the frequency of diarrheal episodes in child care: a randomized, controlled trial. Pediatrics 2000; 105:743-6. 10. Shahid NS, Greenough WB, Samadi AR, Huq MI, Rahman N. Hand washing with soap reduces diarrhoea and spread of bacterial pathogens in a Bangladesh village. J Diar Dis Res 1996;14:85-9. 11. Wilson JM, Chander GN, Muslihatun J. Hand-washing reduces diarrhoea episodes: a study in Lombok, Indonesia. Trans R Soc Trop Med Hyg 1991;85:819-21. 12. Occupational Safety and Health Administration. Occupational exposure to bloodborne pathogens: final rule. Federal Register 1991;29 CFR Part 1910.1030. 13. Arenas MD, Sa´nchez-Paya´ J, Barril G, Garcia-Valdecasas J, Gorriz JL, Soriano A, et al. A multicentric survey of the practice of hand hygiene in haemodialysis units: Factors affecting compliance. Nephrol Dial Transplant 2005;20:1164-71. 14. Pittet D. Improving compliance with hand hygiene in hospitals. Infect Control Hosp Epidemiol 2000;21:381-6.
Shimokura et al 15. O’Boyle CA, Henly SJ, Larson E. Understanding compliance to hand hygiene recommendations: the theory of planned behavior. Am J Infect Control 2001;29:352-60. 16. ESRD facility survey file. Baltimore, MD: Centers for Medicare and Medicaid Services. 1998; updated Nov 6, 2003. Available from: http://www.cms.hhs.gov/esrd/8.asp/. Accessed March 23, 2000. 17. Research Triangle Institute. SUDAAN User’s Manual, Release 8.0. Research Triangle Park, NC: Research Triangle Institute; 2001.
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