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Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307
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Fagernes & lingaas (2011) Factors interfering with the microflora on hands. journal of advanced nursing 67(2), 297 307

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  • 1. JAN JOURNAL OF ADVANCED NURSINGORIGINAL RESEARCHFactors interfering with the microflora on hands: a regression analysis ofsamples from 465 healthcare workersMette Fagernes & Egil LingaasAccepted for publication 13 August 2010Correspondence to M. Fagernes: F A G E R N E S M . & L I N G A A S E . ( 2 0 1 1 ) Factors interfering with the microflora one-mail: mette.fagernes@siv.no hands: a regression analysis of samples from 465 healthcare workers. Journal of Advanced Nursing 67(2), 297–307. doi: 10.1111/j.1365-2648.2010.05462.xMette Fagernes RNPhD StudentDepartment of Internal Medicine, Vestfold AbstractHospital Trust, Tønsberg, Norway and Aims. This paper is a report of a study of the impact of finger rings, wrist watches,Institute of Nursing and Health Sciences, nail polish, length of fingernails, hand lotion, gender and occupation on handUniversity of Oslo, Norway microbiology of healthcare workers. Background. The impact of the above mentioned variables on hand microbiologyEgil Lingaas MD PhD of healthcare workers is not well defined. Large scale studies suitable for multi-Head variate analysis are needed to elucidate their role.Department of Infection Prevention, Methods. Both hands of 465 Norwegian healthcare workers were sampled by theRikshospitalet University Hospital, Oslo, glove juice method during two study periods (2004 and 2007), and examined for totalNorway number of bacteria and presence of Staphylococcus aureus, Enterobacteriacea and non-fermentative Gram-negative rods. Multiple regression analysis was performed. Results. The use of a wrist watch was associated with an enhanced total bacterial count on hands compared to hands without a watch [(B) 3Æ25 (95% CI: 1Æ73–6Æ07), P < 0Æ001], while the use of one plain finger ring increased the carriage rate of Enterobacteriaceae [odds ratio 2Æ71 (95% CI: 1Æ42–5Æ20), P = 0Æ003]. The carriage rate of Staphylococcus aureus was enhanced with fingernails longer than 2 mm [odds ratio 2Æ17 (95% CI: 1Æ29–3Æ66), P = 0Æ004] and after recent use of hand lotion [odds ratio 22Æ52 (95% CI: 4Æ05–125Æ30), P < 0Æ001]. No effect of nail polish was observed. We found an association between occupation and carriage rate of S. aureus and Enterobacteriaceae. Conclusions. Health care workers should remove finger rings and watches at work. Fingernails should be shorter than 2 mm, nail polish may be used. Keywords: hand contamination, hand hygiene, healthcare workers, hospital infection. be frequently transferred by the hands of healthcareIntroduction workers (HCWs). Consequently, hand hygiene is regardedHealth care associated infections (HAI) are major sources of as one of the most fundamental infection preventionmorbidity and mortality worldwide (World Health Organi- practices (Larson 1988, Rotter 2007, World Health Orga-zation 2009). Microorganisms causing HAI are assumed to nization 2009).Ó 2010 Blackwell Publishing Ltd 297
  • 2. M. Fagernes and E. LingaasBackground People were excluded if they had skin irritation or eczema, if they had taken antibiotics during the previous 2 weeks orMany variables may potentially interfere with the risk of had performed surgical hand disinfection during the preced-hand contamination and the effect of hand washing and hand ing 24 hours.disinfection. However, we still lack definitive answers with The following personal and work related data wereregard to the influence of many of these variables, such as nail recorded: gender and occupation, length of fingernails (dom-polish, artificial nails, length of fingernails, wearing of finger inant hand, fourth finger), nail polish (none, intact, chipped),rings and wrist watches, use of hand lotion, gender and artificial nails, finger rings, wrist watch and/or bracelet (onlyoccupation (World Health Organization 2009). Few studies the second study period), hospital, time of day (day,are published on these topics, and the results are partly afternoon or night shift), time since work started, time sincecontradictory. There is a lack of studies suitable for multi- most recent hand washing, hand disinfection and use of handvariate analysis, which is a drawback since many of these lotion, and time since most recent glove use if hand hygienevariables may be highly correlated and require large scale had been omitted after removing gloves.studies to allow independent analysis of each single factor.The inconsistency of the results is reflected in differingrecommendations on these issues in current guidelines on Data collection and microbial methodshand hygiene (Larson 1995, Boyce & Pittet 2002, Pratt et al. The data were collected during two separate study periods in2007, World Health Organization 2009). We therefore need 2004 and 2007 (Fagernes et al. 2007, Fagernes & Lingaasmore data to substantiate the role of these variables in order 2009). Both hands were sampled with a modified version ofto optimize hand hygiene among HCWs. the glove juice method. Each subject inserted their hand into a sterile bag (Stomacher Ò 400 Classic; Seward, Worthing, UK) containing 100 ml of sterile tryptic soy broth withThe study neutralizer as previously described (Fagernes et al. 2007, Fagernes & Lingaas 2009). The bag was occluded around theAims wrist, and the hand was massaged in a standardized mannerThe aim of the present study was to determine the impact of by an investigator for approximately 1 minute. The samplingthe above mentioned variables in a large cohort of HCWs and fluid was collected in a sterile container and total bacterialin ordinary clinical settings by the use of multivariate counts were measured according to the European Norm 1499analysis. (European Committee for Standardization 1997). Staphylo- coccus aureus, Enterobacteriacea and non-fermentative Gram-negative rods (NFGNR) were identified to the speciesStudy design level, but were not quantified. The theoretical sensitivity forWe used a cross-sectional design, appropriate for collecting detection of S. aureus was 500 CFU per hand in study periodempiric data without interfering with the normal behaviour 1, and 90 CFU in study period 2. For detection of Gram-of the study participants. negative rods, the theoretical sensitivity was 1000 CFU per hand in study period 1. In study period 2 a change was made and the sensitivity was 500 CFU per hand for subject 1–58Participants and 10 CFU per hand for subject 59–200.A convenience sample of 465 HCWs directly involved inpatient care (i.e. physicians, nurses, assistants, phlebotomists, Ethical considerationsphysiotherapists and radiography personnel) from three Nor-wegian acute care hospitals were recruited into the study, 265 Participation was voluntary and the HCWs were given oralin study period 1 (2004) and 200 in study period 2 (2007). and written information before consenting to participate. TheThey were interrupted between ordinary clinical work activ- studies were approved by the institutional review board at allities at least 2 hours after starting their shift and asked to hospitals. All data were treated anonymously.participate in the study. The different units were visited atrandom days. No notification was give in advance, and no Data analysisextra hand hygiene was allowed before the hand samples weretaken. HCWs were collected based on the aim to include The median of the average number of bacteria on both handsapproximately the same numbers with and without rings. of each HCW and the presence of S. aureus, Enterobacteri-298 Ó 2010 Blackwell Publishing Ltd
  • 3. JAN: ORIGINAL RESEARCH Variables having an impact on hand contaminationaceae and NFGNR on one or both hands were used as Table 1 Study participants and study variablesoutcome variables. First study Second study To account for the positive skewness of the measured data, period period Totallog-transformed data of total bacterial counts were used in Variable (n = 265) (n = 200) (N = 465)the analysis. Hospital Separate regression models were constructed for total Hospital 1 132 (49Æ8) 155 (77Æ5) 287 (61Æ7)bacterial count (linear regression) and for each organism Hospital 2 133 (50Æ2) 0 (0) 133 (28Æ6)category (logistic regression). For all models, risk factors with Hospital 3 0 (0) 45 (22Æ5) 45 (9Æ7)a P value of <0Æ2 as identified by univariate regression Genderanalyses were incorporated into the multivariable regression Female 243 (91Æ7) 180 (90Æ0) 423 (91Æ0) Male 22 (8Æ3) 20 (10Æ0) 42 (9Æ0)model. The least significant variables were thereafter removed Occupationone by one until all remaining variables had a P £ 0Æ125. Nurse 148 (55Æ8) 114 (57Æ0) 262 (56Æ3)Since the two parts of the study were separated by a period of Nursing assistant 46 (17Æ4) 12 (6Æ0) 58 (12Æ5)approximately 3 years, study number was included in all Phlebotomist 23 (8Æ7) 26 (13Æ0) 49 (10Æ5)models. All explanatory variables were included as categor- Radiography 13 (4Æ9) 17 (8Æ5) 30 (6Æ5) personnelical variables, with the exception of work hours. Physician 11 (4Æ2) 15 (7Æ5) 26 (5Æ6) Use of wrist watches was recorded in the second part of the Physiotherapist 8 (3Æ0) 10 (5Æ0) 18 (3Æ9)study only. A separate analysis was therefore performed for Other 16 (6Æ0) 6 (3Æ0) 22 (4Æ7)this variable. The watch carrying hands were compared with Shifta randomly selected hand of each HCW without a watch, Day shift 236 (89Æ1) 200 (100) 436 (93Æ8)adjusted for hand dominance. Afternoon shift 6 (2Æ3) 0 (0) 6 (1Æ3) Night shift 23 (8Æ7) 0 (0) 23 (4Æ9) The fit of the linear model was assessed by inspection of the Hours at work before samplingresiduals, while the fit of the logistic model was assessed by 3 80 (30Æ2) 62 (31Æ0) 142 (30Æ5)use of the Hosmer and Lemeshow goodness-of-fit test. All 4 56 (21Æ1) 30 (15Æ0) 86 (18Æ5)analyses were performed using the SPSS 16.0 (SPSS Inc., 5 50 (18Æ9) 24 (12Æ0) 74 (15Æ9)Chicago, IL, USA) statistical software package. The level of 6 37 (14Æ0) 50 (25Æ0) 87 (18Æ7) 7 15 (5Æ7) 31 (15Æ5) 46 (9Æ9)statistical significance was set to 5%. >8 27 (10Æ2) 3 (1Æ5) 30 (6Æ5) Finger ring None 113 (42Æ6) 100 (50) 213 (45Æ8)Validity and reliability One plain 121 (45Æ7) 71 (35Æ5) 192 (41Æ3)Hand samples were collected by the ‘Glove juice method’. One decorative 31 (11Æ7) 19 (9Æ5) 50 (10Æ8)The method is considered to be the most valid and reliable More than one 0 (0) 10 (5Æ0) 10 (2Æ2) Wrist watchmethod to describe the transient and permanent flora on No – 121 (60Æ5) 121 (26Æ0)hands (Paulson 1993). Yes – 79 (39Æ5) 79 (17Æ0) Not registered 265 (100) – 265 (57Æ0) Length of fingernails (mm)Results <2 179 (67Æ5) 151 (75Æ5) 330 (71Æ0) 2–2Æ9 65 (24Æ5) 35 (17Æ5) 100 (21Æ5)Hand samples were collected from a total of 465 HCWs. The >3 20 (7Æ5) 9 (4Æ5) 29 (6Æ2)distribution of registered variables is shown in Table 1. Not registered 1 (0Æ04) 5 (2Æ5) 6 (1Æ3) Nail polish No polish 206 (77Æ7) 171 (85Æ5) 377 (81Æ1)Total bacterial count Intact polish 18 (6Æ8) 17 (8Æ5) 35 (7Æ5) Chipped polish 41 (15Æ5) 10 (5Æ0) 51 (11Æ0)The median bacterial count recovered from the hands of 465 Not registered – 2 (1Æ0) 2 (0Æ4)HCWs was 2,075,000 (range 2250–60,500,000). Occupation Artificial nails(P = 0Æ004), finger rings (P = 0Æ002), length of fingernails No 264 (99Æ6) 197 (98Æ5) 461 (99Æ1)(P = 0Æ048), nail polish (P = 0Æ057), time since hand Yes 1 (0Æ4) 3 (1Æ5) 4 (0Æ9)disinfection (P < 0Æ001) and study number (P < 0Æ001) were Minutes since hand washing <5 45 (17Æ0) 25 (12Æ5) 70 (15Æ1)incorporated into the multivariable regression model. As 5–10 65 (24Æ5) 24 (12Æ0) 89 (19Æ1)shown in Table 2, finger rings, time since hand disinfectionÓ 2010 Blackwell Publishing Ltd 299
  • 4. M. Fagernes and E. LingaasTable 1 (Continued) final regression model were hand disinfection, nail length, nail polish and hospital. First study Second study period period TotalVariable (n = 265) (n = 200) (N = 465) Gram negative rods 11–20 62 (23Æ4) 37 (18Æ5) 99 (21Æ3) >20 93 (35Æ1) 114 (57Æ0) 207 (44Æ5) Enterobacteriaceae were found on one or both hands of 75Minutes since hand disinfection (16Æ1%) HCWs. Hospital (P < 0Æ001), occupation <5 13 (4Æ9) 18 (9Æ0) 31 (6Æ7) (P = 0Æ023), gender (P = 0Æ160), finger rings (P = 0Æ027), time 5–10 22 (8Æ3) 23 (11Æ5) 45 (9Æ7) since hand washing (P = 0Æ006) and study number 11–20 18 (6Æ8) 29 (14Æ5) 47 (10Æ1) (P < 0Æ001) were incorporated to the multivariable regression >20 94 (35Æ5) 97 (48Æ5) 191 (41Æ1) model. Gender and time since hand washing were taken out of Not done 118 (44Æ5) 33 (16Æ5) 151 (32Æ5)Minutes since application of hand lotion the model during the multivariate analysis. As shown in <5 9 (3Æ4) 1 (0Æ5) 10 (2Æ2) Table 3, ring wearing was found to have a significant impact 5–10 3 (1Æ1) 2 (1Æ0) 5 (1Æ1) on the recovery of Enterobacteriaceae. Significant differences 11–20 4 (1Æ5) 1 (0Æ5) 5 (1Æ1) were also shown between the three hospitals, study number >20 54 (20Æ4) 42 (21Æ0) 96 (20Æ6) and between nurses and radiography personnel. Not done 195 (73Æ6) 154 (77Æ0) 349 (75Æ1)Minutes since glove use – if hand hygiene had been omitted after Non-fermentative Gram-negative rod species were identi-glove removal fied on one or both hands of 164 (35Æ3 %) of 465 HCWs. <5 5 (1Æ9) 0 (0Æ0) 5 (1Æ1) Hospital (P < 0Æ001), occupation (P = 0Æ167), finger rings 5–10 1 (0Æ4) 1 (0Æ5) 2 (0Æ4) (P = 0Æ049), time since hand disinfection (P = 0Æ127) and 11–20 2 (0Æ8) 1 (0Æ5) 3 (0Æ7) study number (P < 0Æ001) were incorporated in the multi- >20 4 (1Æ5) 3 (1Æ5) 7 (1Æ5) variable regression model. Occupation and finger rings were Not used 253 (95Æ5) 194 (97Æ0) 447 (96Æ1) Not registered – 1 (0Æ5) 1 (0Æ2) taken out of the model during the multivariate analysis, and only hospital, time since hand disinfection and study numberValues are given as n (%). were found to influence the occurrence of NFGNR. Table 4and study number were included in the final model, and were shows effect estimates for the variables in the final model.found to have a significant impact on the total bacterial count. A separate analysis for watches showed an unadjusted A separate analysis of hands with a wrist watch demon- effect on NFGNR carriage [unadjusted effect estimate: ORstrated significantly higher total bacterial counts than on 2Æ21 (95% CI: 1Æ21–4Æ03), P = 0Æ010] which disappearedcontrol hands [unadjusted effect estimate: 5Æ70 (95% CI: after adjusting for finger rings and nail polish in the final3Æ04–10Æ68), P < 0Æ001, adjusted effect estimate: 3Æ25 (95% model [adjusted effect estimate: OR 1Æ34 (95% CI: 0Æ64–CI: 1Æ73–6Æ07), P < 0Æ001]. Variables controlled for in the 2Æ81), P = 0Æ442].Table 2 Multivariate regression analysis of variables with an impact on the total number of bacteria on the hands of healthcare workers(N = 465) Unadjusted effect Adjusted effectVariable (95% CI) P value (95% CI) P valueFinger ring – 0Æ002 – 0Æ003 No ring Reference group – Reference group – One plain ring 1Æ72 (1Æ23–2Æ39) 0Æ001 1Æ40 (1Æ02–1Æ90) 0Æ035 One decorative ring 1Æ82 (1Æ08–3Æ07) 0Æ024 1Æ50 (0Æ92–2Æ43) 0Æ102 More than one ring 3Æ53 (1Æ20–10Æ32) 0Æ022 5Æ53 (2Æ00–15Æ27) 0Æ001Minutes since hand disinfection – <0Æ001 – 0Æ027 Not performed Reference group – Reference group – <5 0Æ23 (0Æ12–0Æ44) <0Æ001 0Æ41 (0Æ22–0Æ77) 0Æ005 5–10 0Æ50 (0Æ29–0Æ87) 0Æ013 0Æ77 (0Æ45–1Æ30) 0Æ329 11–20 0Æ32 (0Æ19–0Æ55) <0Æ001 0Æ56 (0Æ33–0Æ96) 0Æ035 >20 0Æ45 (0Æ31–0Æ64) <0Æ001 0Æ66 (0Æ47–0Æ94) 0Æ020Study period – <0Æ001 – <0Æ001 Study 1 (2004) Reference group – Reference group – Study 2 (2007) 0Æ29 (0Æ21–0Æ39) <0Æ001 0Æ32 (0Æ23–0Æ43) <0Æ001300 Ó 2010 Blackwell Publishing Ltd
  • 5. JAN: ORIGINAL RESEARCH Variables having an impact on hand contaminationTable 3 Multivariate logistic regression analysis of variables with an impact on the occurrence of Enterobacteriaceae on the hands ofhealthcare workers (N = 465) Adjusted ORVariable OR (95% CI) P value (95% CI) P valueHospital – <0Æ001 – 0Æ003 Hospital 1 Reference group – Reference group – Hospital 2 0Æ24 (0Æ10–0Æ57) 0Æ001 0Æ68 (0Æ24–1Æ94) 0Æ470 Hospital 3 4Æ36 (2Æ25–8Æ45) <0Æ001 3Æ47 (1Æ65–7Æ32) 0Æ001Occupation – 0Æ023 – 0Æ076 Nurse Reference group – Reference group – Nursing assistant 0Æ48 (0Æ16–1Æ41) 0Æ182 0Æ55 (0Æ17–1Æ78) 0Æ318 Phlebotomist 1Æ66 (0Æ76–3Æ63) 0Æ202 1Æ24 (0Æ52–2Æ94) 0Æ634 Radiography personnel 3Æ24 (1Æ40–7Æ50) 0Æ006 3Æ98 (1Æ59–10Æ01) 0Æ003 Physician 2Æ39 (0Æ94–6Æ10) 0Æ068 1Æ07 (0Æ36–3Æ16) 0Æ909 Physiotherapist 1Æ85 (0Æ58–5Æ95) 0Æ300 1Æ56 (0Æ44–5Æ55) 0Æ496 Other 1Æ91 (0Æ66–5Æ50) 0Æ232 2Æ20 (0Æ65–7Æ46) 0Æ207Finger ring – 0Æ027 – 0Æ019 No ring Reference group – Reference group – One plain ring 1Æ88 (1Æ08–3Æ28) 0Æ026 2Æ71 (1Æ42–5Æ20) 0Æ003 One decorative ring 1Æ97 (0Æ87–4Æ44) 0Æ102 2Æ25 (0Æ89–5Æ68) 0Æ086 More than one ring 5Æ25 (1Æ38–19Æ94) 0Æ015 2Æ93 (0Æ72–11Æ97) 0Æ133Study period – <0Æ001 – 0Æ001 Study 1 (2004) Reference group – Reference group – Study 2 (2007) 5Æ47 (3Æ10–9Æ70) <0Æ001 3Æ52 (1Æ68–7Æ39) 0Æ001Table 4 Multivariate logistic regression analysis of variables with an impact on the occurrence of non-fermentative Gram-negative rods on thehands of healthcare workers (N = 465) Adjusted ORVariable OR (95% CI) P value (95% CI) P valueHospital – <0Æ001 – <0Æ001 Hospital 1 Reference group – Reference group – Hospital 2 0Æ55 (0Æ34–0Æ88) 0Æ013 0Æ66 (0Æ37–1Æ19) 0Æ165 Hospital 3 10Æ63 (4Æ58–24Æ69) <0Æ001 10Æ02 (4Æ10–24Æ48) <0Æ001Minutes since hand – 0Æ127 – 0Æ021 disinfection Not performed Reference group – Reference group – <5 0Æ35 (0Æ13–0Æ95) 0Æ040 0Æ23 (0Æ08–0Æ70) 0Æ009 5–10 1Æ09 (0Æ55–2Æ17) 0Æ805 0Æ64 (0Æ29–1Æ43) 0Æ280 11–20 0Æ69 (0Æ33–1Æ41) 0Æ307 0Æ37 (0Æ16–0Æ86) 0Æ020 >20 1Æ16 (0Æ75–1Æ81) 0Æ507 0Æ89 (0Æ53–1Æ49) 0Æ657Study period – <0Æ001 – 0Æ092 Study 1 (2004) Reference group – Reference group – Study 2 (2007) 2Æ57 (1Æ74–3Æ80) <0Æ001 1Æ61 (0Æ93–2Æ78) 0Æ092Staphylococcus aureus DiscussionStaphylococcus aureus was detected on one or both hands of Study limitations120 (25Æ8 %) of 465 HCWs. Hospital (P = 0Æ047), occupa-tion (P < 0Æ001), length of fingernails (P = 0Æ010), time since The study includes hand samples from both hands of 465application of hand lotion (P = 0Æ009) and study number HCWs collected in different clinical settings at three Norwe-(P = 0Æ934) were incorporated in the multivariable regression gian acute care hospitals. A cross-sectional design was used.model. Only hospital was removed from the model during the To compensate for the lack of randomization, the differentmultivariate analysis. Table 5 describes effect estimates for units were visited at random days. The results are expected tothe variables in the final model. be generalizable across international hospital settings, butÓ 2010 Blackwell Publishing Ltd 301
  • 6. M. Fagernes and E. LingaasTable 5 Multivariate logistic regression analysis of variables with an impact on the occurrence of Staphylococcus aureus on the hands ofhealthcare workers (N = 459) Adjusted ORVariable OR (95% CI) P value (95% CI) P valueOccupation – 0Æ001 – 0Æ002 Nurse Reference group Reference group Nursing assistant 2Æ46 (1Æ37–4Æ44) 0Æ003 2Æ60 (1Æ39–4Æ90) 0Æ003 Phlebotomist 0Æ59 (0Æ26–1Æ33) 0Æ202 0Æ60 (0Æ26–1Æ38) 0Æ230 Radiography personnel 0Æ22 (0Æ05–0Æ93) 0Æ040 0Æ18 (0Æ04–0Æ82) 0Æ027 Physician 0Æ91 (0Æ35–2Æ36) 0Æ845 1Æ16 (0Æ44–3Æ11) 0Æ762 Physiotherapist 0Æ61 (0Æ17–2Æ16) 0Æ440 0Æ63 (0Æ17–2Æ34) 0Æ492 Other 2Æ53 (1Æ04–6Æ12) 0Æ040 2Æ55 (0Æ98–6Æ66) 0Æ056Length of fingernails (mm) – 0Æ010 – 0Æ014 >2 Reference group – Reference group – 2–2Æ99 2Æ02 (1Æ24–3Æ27) 0Æ005 2Æ17 (1Æ29–3Æ66) 0Æ004 <3 1Æ89 (0Æ84–4Æ24) 0Æ124 1Æ34 (0Æ55–3Æ29) 0Æ518Minutes since use of – 0Æ009 – 0Æ006 hand lotion Not performed Reference group – Reference group – <5 13Æ67 (2Æ85–65Æ69) 0Æ001 22Æ52 (4Æ05–125Æ30) <0Æ001 5–10 2Æ28 (0Æ37–13Æ88) 0Æ372 2Æ28 (0Æ36–14Æ67) 0Æ384 11–20 0Æ85 (0Æ09–7Æ76) 0Æ889 0Æ60 (0Æ060–5Æ99) 0Æ665 >20 1Æ55 (0Æ94–2Æ56) 0Æ084 1Æ38 (0Æ80–2Æ37) 0Æ247Study period – 0Æ934 – 0Æ072 Study 1 (2004) Reference group – Reference group – Study 2 (2007) 1Æ02 (0Æ67–1Æ55) 0Æ934 1Æ54 (0Æ96–2Æ46) 0Æ072potential differences were not explored. It is not known to studies comparing hand microflora of different healthcarewhich degree the results can be generalized to other contexts professionals. Larson (1981) found significantly higher prev-where hygienic aspects of finger rings are of interest, as in alence of Gram negative rods among 31 physicians (42%)kindergartens, food industry etc. than among 54 nurses (9%). Conversely, Horn et al. (1988) found significantly higher prevalence of Gram negative bacteria on the hands of oncology and dermatology nursesGender compared to physicians from the same units. Larson et al.No differences were found between genders, neither regarding (1986) measured total bacterial counts repeatedly among 12bacterial load nor prevalence of potential pathogens. We are nurses and 4 physicians and did not find significant differ-aware of only one previous study comparing the hand ences. Daschner (1985) reported significantly higher bacterialmicroflora of male and female HCWs. Larson (1981) reported numbers and higher prevalence of Gram negative rods and S.significantly higher prevalence of Gram negative rods among aureus on the hands of physicians compared to other HCWs40 male HCWs compared to 63 females. In our study the (N = 328).prevalence of Enterobacteriaceae was 15Æ4% and 23Æ8%among 423 women and 42 men respectively, but the difference Length of fingernailswas not statistically significant (P = 0Æ156). Multivariate analysis demonstrated a statistically significant correlation between fingernails longer than 2 mm andOccupation prevalence of S. aureus, but no association with carriageUsing nurses as reference, nursing assistants had higher of Gram negative rods or total bacterial numbers. We havecarriage rate of S. aureus, whereas the prevalence was lower identified two published studies on the influence of theamong radiography personnel. The latter group, however, length of natural nails. Rupp et al. (2008) examined 192more frequently carried Enterobacteriaceae. No differences samples from the dominant hand of 69 nurses over a 2-yearwere found in total bacterial counts between nurses and other period and found increased bacterial counts with nail lengthoccupational groups. We have identified four published above 2 mm, but no difference in the recovery of Gram302 Ó 2010 Blackwell Publishing Ltd
  • 7. JAN: ORIGINAL RESEARCH Variables having an impact on hand contaminationnegative enteric bacteria. By swabbing the front of the watches on the bacterial counts on the wrist and finger tips.fingernails on the dominant hand of 100 nurses, including They found that watch wearers had higher counts of bacteriathe cuticle area, Wynd et al. (1994) were not able to detect on their wrist compared to HCWs without a wrist watch.an influence of nail length on total bacterial numbers. They did not find any impact of wrist watches on theNeither of these two studies reported the prevalence of bacterial load on finger tips when the watch was kept inS. aureus. place. When the HCW removed the watch prior to sampling, Recommendations on length of fingernails vary in different the manipulation of the watch resulted in increased counts ofguidelines for hand hygiene. Some guidelines use the phrase bacteria on the fingertips (Jeans et al. 2010).short nails (Pratt et al. 2007), whereas Centers for Disease In the present study, we recovered more than three times asControl and Prevention (CDC) (Boyce & Pittet 2002) and the many bacteria from hands with watches compared to controlWorld Health Organization (WHO) (World Health Organi- hands. We recommend that HCW abstain from the use ofzation 2009) recommend nail length less than 1/4-inch wrist watches at work.(6Æ3 mm), and 5 mm respectively. Based on the findings ofthe present study and the results of Rupp et al. (2008), we Finger ringsrecommend that the fingernails of HCWs should not belonger than 2 mm. The overall analysis showed that HCWs with finger rings had enhanced total number of bacteria on hands. However, we suspect that this finding is due to the lack of adjustment forNail polish watches in the aggregated 2004/2007 data. Watches wereNo impact of nail polish was detected in this study. We are not shown to significantly increase bacterial numbers in the 2007aware of any other study examining the impact of nail polish study, which also demonstrated a significant correlationon the microflora of the whole hand. Three studies, sampling between the use of rings and watches; 64% of ring wearersthe nails only, did not show any influence of polish on used a wrist watch compared to 15% of the HCW withoutbacterial counts before hand hygiene (Baumgardner et al. ring.1993, Wynd et al. 1994, Edel et al. 1998). However, two For Enterobacteriaceae a significant increase in prevalencestudies with 100 and 61 participants respectively demon- was revealed for one plain ring only. We assume that thestrated higher counts on polished nails after surgical scrub failure to detect a significant effect of a single decorative ring(Wynd et al. 1994, Edel et al. 1998). The third study did not and multiple rings is due to insufficient statistical power.detect differences after regular hand washing in 26 partici- These two groups were much smaller than the groups with apants with nail polish on one hand only (Baumgardner et al. single plain ring and no ring. No influence of rings was1993). Among the guidelines cited above, only the UK detected for S. aureus or NFGNR.guideline recommends that HCWs refrain from using nail We have identified more than 20 studies on the influence ofpolish. Our results do not support this recommendation. finger rings published in scientific journals since 1968 (Lowbury et al. 1968, Nicholson-Pegg 1982, Dewan & Fergus 1985, Hoffman et al. 1985, Jacobson et al. 1985,Artificial fingernails Athar et al. 1989, Field et al. 1996, Nicolai et al. 1997,Due to low numbers, wearing of artificial fingernails was not Salisbury et al. 1997, Trick et al. 2003, Alp et al. 2006,incorporated in the regression analysis. Kelsall et al. 2006, Waterman et al. 2006, Fagernes & Nord 2007, Fagernes et al. 2007, Wongworawat & Jones 2007, Al-Allak et al. 2008, Rupp et al. 2008, Yildirim et al. 2008,Wrist watches Alur et al. 2009, Fagernes & Lingaas 2009, Stein &The guidelines from CDC and WHO do not address the issue Pankovich-Wargula 2009, Hautemaniere et al. 2010). Mostof wrist watches, except before surgical hand antisepsis of these studies conclude that there is an association between(Boyce & Pittet 2002, World Health Organization 2009), ring wearing and an enhanced bacterial load on hands, andwhile the English guideline state that wrist jewellery should an increased prevalence of Gram negative bacteria. Resultsbe removed prior to patient contact (Pratt et al. 2007). Only from studies of the association between rings and handtwo studies have previously been published on this issue. contamination after hand hygiene are less consistent. InField et al. (1996) found that skin below wrist watches particular, several studies failed to show differences afterharbours more bacteria than control skin on the opposite surgical hand antisepsis (Jacobson et al. 1985, Watermanwrist. Jeans et al. (2010) investigated the impact of wrist et al. 2006, Wongworawat & Jones 2007).Ó 2010 Blackwell Publishing Ltd 303
  • 8. M. Fagernes and E. Lingaas Hand lotion What is already known about this topic Guidelines on hand hygiene commonly recommend frequent • Healthcare associated infections are universal and their use of hand lotion to maintain the integrity of the skin prevention has high priority in healthcare facilities (Larson 1995, Boyce & Pittet 2002, World Health Organi- worldwide. zation 2009). We found a significant association between the • Even though hand hygiene is widely accepted as a use of hand lotion within 5 minutes before sampling and cornerstone of infection prevention, we still lack recovery of S. aureus. One possible explanation for this answers to several questions on how to optimize hand finding may be that the hands pick up staphylococci more hygiene. efficiently immediately after application of hand lotion. • Due to lack of valid information, international and However, it may be due to better recovery or enhanced national guidelines on hand hygiene (WHO, UK, US dispersion of S. aureus during sampling and plating due to the and others) differ in their recommendations regarding influence of surface-active ingredients, or simply to statistical ring wearing, use of wrist watches, nail length and nail chance. In a paper by Jacobson et al. (1985), reporting polish. bacterial counts on the hands of 12 volunteers, the authors note that they observed that hand lotion increased the What this paper adds bacterial count. However, no data were presented, and no follow-up has been published. Further studies are needed on • Wrist watches and finger rings are associated with this issue. increased bacterial numbers on the hands of healthcare workers. • Long finger nails (>2 mm) enhance the carriage rate of Hand washing and hand disinfection Staphylococcus aureus. There is a plethora of published studies on the efficacy of • Nail polish has no impact on hand contamination, while different methods and agents for hand decontamination. the use of hand lotion may increase the carriage rate of However, the present study is not a study of the immediate Staphylococcus aureus. effect of hand hygiene. It is a cross-sectional study taking into account the time since hand washing or hand disinfection, Implications for practice and/or policy and also the risk of recontamination during ordinary health- care activities between performance of hand hygiene and • Healthcare workers should keep finger nails short sampling. We found a significant reduction of total bacterial (<2 mm), and remove all finger rings (included plain load on hands among HCW who had previously performed wedding rings) and wrist watches during clinical work. hand antisepsis with alcohol, but no effect of previous hand • Several guidelines on hand hygiene should be re-written washing even within 5 minutes before sampling. As the risk with regard to length of fingernails and the use of wrist of recontamination is probably independent of the method watches, finger rings and nail polish. used for previous hand hygiene, this difference is most • Educational and clinical leaders must give a priority to probably a result of a sustained effect of alcohol on the implementation and compliance to the guidelines on permanent microflora. A somewhat complex correlation was hand hygiene. found between the total number of bacteria recovered and the time since hand disinfection. Compared to HCWs who had not disinfected their hands on the day of sampling, a The CDC states that no recommendation can be made significant reduction of bacterial load was observed for allabout wearing rings in healthcare settings, and that this is an 5-minute intervals after disinfection, except for samplesunresolved issue (Boyce & Pittet 2002). WHO recommends collected between 5 and 10 minutes after hand disinfection.the removal of rings or other jewellery during health care, but Most probably this is due to chance, even though this groupaccept the use of simple wedding band during routine care is statistically similar to the other groups (subject numbers,based on strong religious or cultural influences (World Health CFU range). A possible explanation might be that alcohol hasOrganization 2009). UK guidelines issued in 2007 state that a biphasic effect on hand microflora with an initial reversibleall wrist an ideally hand jewellery should be removed before a bacteriostatic effect followed by a slower bactericidal effect.shift of clinical work begins (Pratt et al. 2007). Our results Previous hand disinfection was also associated with asupport this recommendation. reduced prevalence of NFGNR. This is probably due to a304 Ó 2010 Blackwell Publishing Ltd
  • 9. JAN: ORIGINAL RESEARCH Variables having an impact on hand contaminationsustained effect on the permanent skin flora, which frequently Fundingcontains NFGNR (Lucet et al. 2002). In contrast, Entero-bacteriaceae and S. aureus, which are more typical represen- The study was funded by research grants from Helse Sørtatives of temporary bacteria, were not affected by previous RHF, Norway, which is a public hospital trust.disinfection. This may be due to contamination of the handsin the time interval between hand disinfection and sampling. Conflict of interest No conflict of interest has been declared by the authors.Differences between the two study periodsWe found significantly lower bacterial load on hands in the Author contributionssecond study period. This can probably be explained by asignificant increase in the use of alcoholic hand disinfection MF and EL were responsible for the study conception andfrom the first to the second study period. Also, a significantly design. MF performed the data collection. MF performed thehigher prevalence of Gram negative bacteria was observed, data analysis. MF and EL were responsible for the drafting ofwhich may be a result of enhanced sensitivity of the detection the manuscript. MF and EL made critical revisions to themethod. These differences are taken into consideration in the paper for important intellectual content. MF providedregression analysis by including study period as an indepen- statistical expertise. MF obtained funding. MF and ELdent variable. provided administrative, technical or material support. EL supervised the study.Conclusion ReferencesDue to lack of valid information about variables with apotential impact on hand microflora, current guidelines on Al-Allak A., Sarasin S., Key S. & Morris-Stiff G. (2008) Weddinghand hygiene have differing recommendations on these issues rings are not a significant source of bacterial contamination following surgical scrubbing. Annals of the Royal College of(Larson 1995, Boyce & Pittet 2002, Pratt et al. 2007, World Surgeons of England 90(2), 133–135.Health Organization. 2009). The present study includes hand Alp E., Haverkate D. & Voss A. (2006) Hand hygiene among labo-samples from both hands of 465 HCW, and is to our ratory workers. Infection Control and Hospital Epidemiologyknowledge the largest study on this subject. The results show 27(9), 978–980.that neither wrist watches nor rings should be used by Alur A.A., Rane M.J., Scheetz J.P., Lorenz D.J. & Gettleman L.healthcare workers at work, and that fingernails should not (2009) Simulated microbe removal around finger rings using dif- ferent hand sanitation methods. International Journal of Oralbe longer than 2 mm. Nail polish does not seem to influence Science 1(3), 136–142.the microflora on hands, but hand lotion may be a risk factor Athar M.A., Stafford L. & Wootliff J.S. (1989) Bacterial populationand needs to be further examined. of ring and control fingers in health care workers. Infection It is a responsibility both for the individual healthcare Control Canada 4(2), 8–12.worker and the healthcare institutions to ensure patient safety Baumgardner C.A., Maragos C.S., Walz J. & Larson E. (1993) Effects of nail polish on microbial growth of fingernails. Dispellingbased on evidence based practice. Several international, sacred cows. AORN Journal 58(1), 84–88.national and institutional guidelines on hand hygiene should Boyce J.M. & Pittet D. (2002) Guideline for Hand Hygiene inbe re-written with regard to length of fingernails and the use Health-Care Settings: recommendations of the Healthcare Infec-of wrist watches, finger rings and nail polish. Implementation tion Control Practices Advisory Committee and the HICPAC/of the guidelines should been given priority by both educa- SHEA/APIC/IDSA Hand Hygiene Task Force. Infection Controltional and clinical leaders. and Hospital Epidemiology 23(12 Suppl.), 3–40. Daschner F.D. (1985) The transmission of infections in hospitals by staff carriers, methods of prevention and control. Infection ControlAcknowledgements 6(3), 97–99. Dewan P.A. & Fergus M. (1985) Rings in operating theatres. NewWe greatly appreciate statistical advice from Magne Thore- Zealand Medical Journal 98(793), 1094.sen. We also thank Tone Herring, Hilde Kaasa, Anne Edel E., Houston S., Kennedy V. & LaRocco M. (1998) Impact of a 5-minute scrub on the microbial flora found on artificial, polished,Ottestad Syvertsen, Terje Lingaas and Trond Lingaas for or natural fingernails of operating room personnel. Nursingtechnical assistance and May-Solveig Fagermoen for valuable Research 47(1), 54–59.comments in the introductory part of this study. We are European Committee for Standardization (1997) European Commit-grateful to all HCW participating in the study. tee for Standardization. Chemical Disinfectants and Antiseptics –Ó 2010 Blackwell Publishing Ltd 305
  • 10. M. Fagernes and E. Lingaas Hygienic Handwash – Test Methods and Requirements. Phase 2/ and after different hand hygiene techniques: a randomized clinical Step 2. European Committee for Standardization, Brussels, Belgium. trial. Journal of Hospital Infection 50(4), 276–280.Fagernes M. & Lingaas E. (2009) Impact of finger rings on trans- Nicholson-Pegg A. (1982) The wearing of wedding rings in the mission of bacteria during hand contact. Infection Control and operating department. NATNEWS 19(4), 19–25. Hospital Epidemiology 30(5), 427–432. Nicolai P., Aldam C.H. & Allen P.W. (1997) Increased awareness ofFagernes M. & Nord R. (2007) A study of microbial load of different glove perforation in major joint replacement. A prospective, ˚ types of finger rings worn by healthcare personnel. Vard i Norden randomised study of Regent Biogel Reveal gloves. Journal of Bone 27(2), 21–24. and Joint Surgery. British Volume 79(3), 371–373.Fagernes M., Lingaas E. & Bjark P. (2007) Impact of a single plain Paulson D.S. (1993) Evaluation of three microorganism recovery finger ring on the bacterial load on the hands of healthcare procedures used to determine handwash efficacy. Dairy, Food and workers. Infection Control and Hospital Epidemiology 28(10), Environmental Sanitation 13(9), 520–523. 1191–1195. Pratt R.J., Pellowe C.M., Wilson J.A., Loveday H.P., Harper P.J.,Field E.A., McGowan P., Pearce P.K. & Martin M.V. (1996) Rings Jones S.R., McDougall C. & Wilcox M.H. (2007) epic2: National and watches: should they be removed prior to operative dental evidence-based guidelines for preventing healthcare-associated procedures? Journal of Dentistry 24(1–2), 65–69. infections in NHS hospitals in England. Journal of HospitalHautemaniere A., Cunat L., Diguio N., Vernier N., Schall C., Daval Infection 65(Suppl. 1), S1–S64. M., Ambrogi V., Tousseul S., Hunter P.R. & Hartemann P. (2010) Rotter M.L. 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Microbial flora on the hands of health care personnel: differences Salisbury D.M., Hutfilz P., Treen L.M., Bollin G.E. & Gautam S. in composition and antibacterial resistance. Infection Control and (1997) The effect of rings on microbial load of health care workers’ Hospital Epidemiology 9(5), 189–193. hands. American Journal of Infection Control 25(1), 24–27.Jacobson G., Thiele J.E., McCune J.H. & Farrell L.D. (1985) Stein D.T. & Pankovich-Wargula A.L. (2009) The dilemma of the Handwashing: ring-wearing and number of microorganisms. wedding band. Orthopedics 32(2), 86. Nursing Research 34(3), 186–188. Trick W.E., Vernon M.O., Hayes R.A., Nathan C., Rice T.W.,Jeans A.R., Moore J., Nicol C., Bates C. & Read R.C. (2010) Peterson B.J., Segreti J., Welbel S.F., Solomon S.L. & Weinstein Wristwatch use and hospital-acquired infection. Journal of R.A. (2003) Impact of ring wearing on hand contamination and Hospital Infection 74(1), 16–21. comparison of hand hygiene agents in a hospital. 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American Journal of Infection World Health Organization (2009) Who Guidelines on Hand Hygiene Control 23(4), 251–269. in Health Care. World Health Organization, Geneva, Switzerland.Larson E., McGinley K.J., Grove G.L., Leyden J.J. & Talbot G.H. Wynd C.A., Samstag D.E. & Lapp A.M. (1994) Bacterial carriage (1986) Physiologic, microbiologic, and seasonal effects of hand- on the fingernails of OR nurses. AORN Journal 60(5), 796, 799– washing on the skin of health care personnel. American Journal of 805. Infection Control 14(2), 51–59. Yildirim I., Ceyhan M., Cengiz A.B., Bagdat A., Barin C., Kutluk T.Lowbury E.J.L., Blowers R. & Cunliff A.C. (1968) Aseptic methods & Gur D. (2008) A prospective comparative study of the rela- in the operating suite. Lancet 1, 705–709. tionship between different types of ring and microbial hand colo-Lucet J.C., Rigaud M.P., Mentre F., Kassis N., Deblangy C., nization among pediatric intensive care unit nurses. International Andremont A. & Bouvet E. 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  • 11. JAN: ORIGINAL RESEARCH Variables having an impact on hand contamination The Journal of Advanced Nursing (JAN) is an international, peer-reviewed, scientific journal. JAN contributes to the advancement of evidence-based nursing, midwifery and health care by disseminating high quality research and scholarship of contemporary relevance and with potential to advance knowledge for practice, education, management or policy. JAN publishes research reviews, original research reports and methodological and theoretical papers. For further information, please visit JAN on the Wiley Online Library website: www.wileyonlinelibrary.com/journal/jan Reasons to publish your work in JAN: • High-impact forum: the world’s most cited nursing journal and with an Impact Factor of 1Æ518 – ranked 9th of 70 in the 2010 Thomson Reuters Journal Citation Report (Social Science – Nursing). JAN has been in the top ten every year for a decade. • Most read nursing journal in the world: over 3 million articles downloaded online per year and accessible in over 7,000 libraries worldwide (including over 4,000 in developing countries with free or low cost access). • Fast and easy online submission: online submission at http://mc.manuscriptcentral.com/jan. • Positive publishing experience: rapid double-blind peer review with constructive feedback. • Early View: rapid online publication (with doi for referencing) for accepted articles in final form, and fully citable. • Faster print publication than most competitor journals: as quickly as four months after acceptance, rarely longer than seven months. • Online Open: the option to pay to make your article freely and openly accessible to non-subscribers upon publication on Wiley Online Library, as well as the option to deposit the article in your own or your funding agency’s preferred archive (e.g. PubMed).Ó 2010 Blackwell Publishing Ltd 307

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