impact of finger rings on transmission of bacteria during hand contact •

Impact of Finger Rings on Transmission of Bacteria During Hand Contact • Author(s): Mette Fagernes, RN, Cand.san; Egil Lingaas, PhDSource: Infection Control and Hospital Epidemiology, Vol. 30, No. 5 (May 2009), pp. 427-432Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiologyof AmericaStable URL: http://www.jstor.org/stable/10.1086/596771 .

Accessed: 18/05/2014 23:50

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

The University of Chicago Press and The Society for Healthcare Epidemiology of America are collaboratingwith JSTOR to digitize, preserve and extend access to Infection Control and Hospital Epidemiology.

http://www.jstor.org

This content downloaded from 195.78.108.143 on Sun, 18 May 2014 23:50:51 PMAll use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=ucpress

http://www.jstor.org/action/showPublisher?publisherCode=shea

http://www.jstor.org/action/showPublisher?publisherCode=shea

http://www.jstor.org/stable/10.1086/596771?origin=JSTOR-pdf

http://www.jstor.org/page/info/about/policies/terms.jsp


infection control and hospital epidemiology may 2009, vol. 30, no. 5

o r i g i n a l a r t i c l e

Impact of Finger Rings on Transmission of BacteriaDuring Hand Contact

Mette Fagernes, RN, Cand.san; Egil Lingaas, PhD

objective. To investigate the impact of finger rings on the transmission of bacteria from the hands of healthcare workers and theimpact on the microflora on the hands of healthcare workers in clinical practice.

design. Our study had a nonequivalent control group posttest-only design (pre-experimental). Healthcare workers who wore fingerring(s) on 1 hand and no ring on the other hand ( ) and a control group of healthcare workers who did not wear any ringsn p 100( ) exchanged standardized hand shakes with an investigator wearing sterile gloves. Samples from the gloved hands of the investigatorsn p 100and the bare hands of the healthcare workers were thereafter obtained by the glove juice technique.

setting. Two Norwegian acute care hospitals.

participants. Healthcare workers ( ) during ordinary clinical work.n p 200

results. A significantly higher bacterial load (odds ratio, 2.63 [95% confidence interval, 1.28–5.43]; ) and a significantly higherP p .009number of bacteria transmitted (odds ratio, 2.43 [95% confidence interval, 1.44–4.13]; ) were associated with ringed hands,P p .001compared with control hands. However, a multiple analysis of covariance revealed no statistically significant effect of rings alone. Theprevalence of nonfermentative gram-negative bacteria (42% vs 26%) and Enterobacteriaceae (26% vs 13%) was also significantly higheramong persons who wore rings than among persons who did not wear rings. However, no statistically significant differences in the incidenceof transmission of these pathogens were detected after hand contact. The prevalence of Staphylococcus aureus and incidence of transmissionof S. aureus were the same in both groups.

conclusions. Wearing finger rings increases the carriage rate of nonfermentative gram-negative bacteria and Enterobacteriaceae on thehands of healthcare workers. However, no statistically significant differences in the incidence of transmission of nonfermentative gram-negative bacteria or Enterobacteriaceae were detected between the healthcare workers who wore rings and those who did not.

Infect Control Hosp Epidemiol 2009; 30:427-432

From the Institute of Nursing and Health Sciences, University of Oslo (M.F.), and Department of Infection Prevention, Rikshospitalet University Hospital(E.L.), Oslo, Norway

Received August 6, 2008; accepted December 8, 2008; electronically published April 2, 2009.� 2009 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2009/3005-0004$15.00. DOI: 10.1086/596771

Contaminated hands and inferior hand hygiene amonghealthcare workers (HCWs) are considered to contribute sig-nificantly to the spread of healthcare-associated infections.Despite some contradictory results in previous studies,1-15 ringwearing is assumed to have an impact on the bacterial loadon the hands and to increase the rate of carriage of potentiallypathogenic bacteria, such as Staphylococcus aureus and gram-negative bacteria.

In a previous study, we reported that HCWs who woreplain finger rings more frequently carried Enterobacteriaceaespecies on their hands than did HCWs who did not wearrings, but we did not find a statistically significant differencein total bacterial load or carriage rate of S. aureus or non-fermentative gram-negative bacteria.1 To our knowledge, ourstudy1 and the study by Trick et al.6 are the only studies thathave investigated the impact of finger rings on the bacterialflora on the hands of HCWs in regular clinical settings. How-

ever, to our knowledge, no study on the correlation betweenring wearing and transmission of bacteria from hands hasbeen published, and the question still remains whether ringsenhance the risk of transmission from the hands of HCWsto patients, medical devices, or the environment.

Therefore, the main objective of the present study was toexamine the impact of finger rings on the transmission ofbacteria from the hands of HCWs. We also aimed to repeatour previous study of the impact on the microflora on thehands of HCWs in clinical practice in a modified manner,including HCWs wearing decorative rings and multiple rings.

methods

Design

The present study had a nonequivalent control group post-test-only design (pre-experimental).



428 infection control and hospital epidemiology may 2009, vol. 30, no. 5

Participants

HCWs who were directly involved in patient care (physicians,nurses, nursing assistants, phlebotomists, physiotherapists,and radiography personnel) at 2 Norwegian acute care hos-pitals were recruited into the study. Eligible participants werepersonnel who wore at least 1 ring on 1 hand and no ringon the other hand and personnel who did not wear any rings.For inclusion in the study, the participants should have beenat work with regular patient contact for at least 2 hours beforeobtainment of bacteriological samples. No notification wasgiven in advance. With the exception of some phlebotomists,participants were approached in the corridors on their wayto or from patient rooms, medicine rooms, clean stores, andother areas. This was done to obtain samples from the handswithout interfering with normal hand hygiene practice. Noextra hand hygiene was allowed before the hand samples wereobtained. The rings were left in place, but wrist watches wereremoved before samples were obtained to avoid damagecaused by the sampling solution. Participation was voluntary,and participants were given oral and written information be-fore consenting to participate. The study was reviewed andapproved by the institutional review boards at both hospitals.All data were treated anonymously.

The following personal and work-related data were re-corded for each HCW: sex, length of finger nails (in mm),nail polish (none, intact, or chipped), artificial nails, wristwatch and/or bracelet(s), occupation, hospital, unit, time ofday (day shift, afternoon shift, or night shift), number ofhours since work started, estimated time since most recenthand washing and hand disinfection, time since most recentuse of gloves if hand hygiene had been omitted after gloveremoval, and time since most recent use of hand emollient.HCWs were excluded if they had skin irritation or eczema,if they had received antibiotic therapy during the previous 2weeks, or if they had performed surgical hand disinfectionduring the previous 24 hours. With the exception of surgicalscrub, only nonmedicated soap and 70% ethanol were avail-able for hand hygiene in the hospitals. Each person was in-cluded only once.

Microbiology

Microbiological transmission during hand contact was mea-sured using a recently developed model.16 In short, the HCWshook both hands in a standardized manner with an inves-tigator wearing sterile gloves (and gown), applying moderatefriction for approximately 30 seconds. For the sake of stan-dardization, the investigator was the same person in all cases.Samples were thereafter obtained from the gloved hands ofthe investigator and the bare hands of the HCW with use ofthe glove juice technique. In short, the hand of the participantwas placed in a sterile bag with 100 mL of sampling solutionand was massaged in a standardized manner by an investi-gator (other than the investigator who shook the HCW’shand).

The specimens were processed in the laboratory within 2hours after they were obtained. Laboratory personnel wereunaware of all hand characteristics. The samples were vor-texed for 1 minute before microbiological examination wasperformed. All plates were incubated for 48 hours at 35�C.

Total bacterial load. Sampling solutions from bare handswere serially diluted by 10-fold, up to , in tryptic�31 # 10soy broth with neutralizers (30 mL polysorbate 80, 1 g his-tidine, 5 g sodium thiosulphate, and 1 g lyophilized bovineserum albumin per 1000 mL). Aliquots of 100 mL from eachdilution were spread onto human blood agar plates and tryp-tone soya agar plates. Sampling solutions from the glovedhands of recipients were not diluted, but aliquots of 100 mLwere spread directly on blood agar plates and tryptone soyaagar plates, and aliquots of 2 mL and 20 mL were also filteredthrough a 0.45-mm filter (Millipore S.A.) and placed on bloodagar plates. Total bacterial loads were calculated from a meanof the agar plates in accordance with the procedure describedin European Norm 1499.17

S. aureus. For detection of S. aureus in samples from barehands, 100 mL of undiluted sampling solution was spread onmannitol salt agar plates, and 1 mL was placed in 9 mL ofmannitol salt broth. One milliliter of the sampling solutionfrom the gloved hands of recipients were added to 9 mL ofmannitol salt broth, and another 10 mL were filtered andplaced on mannitol salt agar plates. S. aureus was identifiedto the species level by Staphaurex Plus Latex Test (RemelEurope) and the tube coagulase test. Isolates were only notedas present or absent and were not quantified. The theoreticalsensitivities for detection of S. aureus on HCW and inves-tigator hands were 90 colony-forming units (CFU) per handand 9 CFU per hand, respectively.

Gram-negative bacteria. Aliquots of 100 mL from the un-diluted solutions of samples obtained from the bare handsof HCWs were spread on lactose bromthymol agar plates,with and without the addition of vancomycin (7.5 mg/L forselective culture of gram-negative bacteria). For detection ofgram-negative bacteria in samples from the gloved hands ofinvestigators, two 10-mL aliquots were filtered and placed onlactose bromthymol agar plates with and without vancomycin(1 each). Gram-negative bacteria were identified to the specieslevel by Vitek 2 (bioMerieux). Isolates were only noted aspresent or absent and were not quantified. The theoreticalsensitivities for detection of gram-negative bacteria on HCWand investigator hands were 500 CFU per hand and 5 CFUper hand, respectively.

Statistical Methods

To account for the positive skewness in the measured data,group values were compared by Student’s t test with use ofnatural logarithm–transformed data. The ringed hand ofHCWs who wore rings was compared with a randomly se-lected hand in the group of HCWs without rings; adjustmentwas made for hand dominance. The Wilcoxon signed rank



finger rings and transmission of bacteria 429

table 1. Bacterial Loads Recovered from the Hands of Healthcare Workers (HCWs) Withand Without Rings and from the Hands of Investigators

Study group, hand

Bacterial load on hands of HCWsTransmitted bacterial loadon hands of investigators

Median (IQR) CFU P a Median (IQR) CFU P a

HCWs with ring(s)Hand with ring(s) 1,336,250 (287,500–3,780,833) .795 1,800 (679–5,925) .198Hand without ring 1,305,000 (275,000–3,437,500) 2,075 (1,028–6,750)

HCWs without ringsDominant hand 547,500 (95,750–2,412,500) .848 1,000 (261–2,955) .624Nondominant hand 467,500 (71,250–1,840,000) 755 (184–2,925)

note. There were 100 HCWs in each study group. In a nonpaired analysis comparing the ringed handsof HCWs with a ring(s) with 1 random hand of an HCW without a ring (adjusting for hand dominance)with use of Student’s t test and natural logarithm–transformed data, for bacterial loads on handsP p .009of HCWs and for bacterial load on hands of investigators. CFU, colony-forming units; IQR,P p .001interquartile range.a By paired analysis with Wilcoxon signed rank test.

test was used for the paired comparison of hands of HCWswith a ring(s) on 1 hand. Pearson’s r coefficient was used forinvestigation of the correlation between the bacterial load onthe hands of HCWs and the bacterial load transmitted to thehands of recipients during standardized hand contact.

To estimate the effect of possible confounding variables onthe total bacterial load, an analysis of covariance was per-formed. All variables with an unadjusted estimated P !

were incorporated into the model. Thereafter, backward.200elimination was performed in which variables with high Pvalues were removed from the model, 1 by 1. Unless theparameter estimate of the main effect variable (study group)changed by more than 20%, the variable was excluded fromthe final model. Variables with were included inP X .125the final model.

Categorical variables were compared using either Mc-Nemar‘s test or the Pearson x2 test. Logistic regression analysiswas performed to estimate the influence of possible con-founding variables on the occurrence of potential pathogens,as determined by analysis of covariance.

All analyses were performed using SPSS, version 16.0 (SPSS).The level of statistical significance was set at .P p .05

results

A total of 200 HCWs were included in the present study; 100wore a ring(s) on 1 hand only, and 100 did not wear anyrings (control subjects). One hundred fourteen (57.0%) ofthe participants were nurses, 26 (13.0%) were phlebotomists,17 (8.5%) were radiography personnel, 15 (7.5%) were phy-sicians, 12 (6.0%) were nursing assistants, 10 (5.0%) werephysiotherapists, and 6 (3.0%) were other healthcare profes-sionals. One hundred eighty participants (90.0%) werewomen.

Of the 100 HCWs who wore rings, 71 wore 1 plain ring,19 wore 1 decorative ring, and 10 wore more than 1 ring. Awrist watch was worn by 79 HCWs (39.5%), and a bracelet

was worn by 3 HCWs (1.5%). One hundred fifty-one HCWs(75.5%) had finger nails that were shorter than 2 mm,whereas 35 (17.5%) had nails with a length of 2–2.9 mm,and 14 (7.0%) had nails that were longer than 3 mm. Only3 participants (1.5%) had artificial finger nails. Seventeenparticipants (8.5%) had intact nail polish, 10 (5.0%) hadchipped nail polish, and 171 (85.5%) had no nail polish.

Thirty-three participants (16.5%) had not used any handdisinfectant on the day that the sample was obtained. Ninety-seven (48.5%) reported that they had disinfected their handswith alcohol more than 20 minutes before the sample wasobtained, whereas 29 (14.4%) reported that they had disin-fected their hands 11–20 minutes before the sample was ob-tained and 23 (11.5%) reported that they had disinfected theirhands 5–10 minutes before the sample was obtained. Eighteenparticipants (9.0%) had performed hand disinfection withinthe 5 minutes before the sample was obtained.

The 2 study groups were found to be comparable withregard to all registered, potentially confounding variables,with the exception of occupation and use of wrist watches.Sixty-four (64.0%) of the HCWs who wore rings were wearinga wrist watch, compared with 15 (15.0%) of the control sub-jects ( , Pearson x2 test). There were significantly moreP ! .001physicians in the ring group than in the control group( , Pearson x2 test).P ! .001

Total Bacterial Load

The total bacteria loads recovered from the HCWs and in-vestigators in the different study groups are shown in Table1. The median bacterial load recovered from all bare handscombined ( ) was 907,500 CFU (range, 0–73,500,000n p 400CFU). Significantly higher bacteria loads were recovered fromthe hands of participants with rings than from the hands ofcontrol subjects (Table 1), but no statistically significant dif-ferences were found between the hands with and without aring(s) among the individuals who wore rings. However, an




table 2. Unadjusted and Adjusted Estimates of the Effect ofFinger Rings on Bacterial Loads on the Hands of Healthcare Work-ers With Rings and on the Hands of Investigators

Results

Effect of rings onbacterial load on hands

Effect of ringson transmission

of bacteria from hands

OR (95% CI) P OR (95% CI) P

Unadjusted 2.63 (1.28–5.43) .009 2.43 (1.44–4.13) .001Adjusted 1.7 (0.83–3.65) .142 1.31 (0.76–2.27) .326

note. Variables incorporated in the final regression model were wristwatches, hand disinfection, nail length, and nail polish in the analysis forthe effect of rings on bacterial load on hands and wrist watches, sex, handdisinfection, and nail polish in the analysis of the effect of rings on trans-mission of bacteria from hands. CI, confidence interval; OR, odds ratio.

table 3 Impact of Finger Rings on the Prevalence and Transmission of Gram-Negative Bacteria

Bacteria

Presence of gram-negative bacteria on ringed hands Transmission of gram-negative bacteria from ringed hands

OR (95% CI) P Adjusted OR (95% CI) P OR (95% CI) P Adjusted OR (95% CI) P

One or more speciesof gram-negativebacteria 1.926 (1.09–3.39) .023 2.411 (1.13–5.13) .022 2.348 (0.79–7.03) .127 2.207 (0.72–6.79) .167

Enterobacteriaceae 2.351 (1.13–4.90) .022 2.228 (1.05–4.75) .038 1.515 (0.25–9.27) .653 NDNonfermentative gram-

negative bacteria 2.061 (1.13–3.75) .018 2.143 (1.06–4.19) .026 2.37 (0.71–7.98) .162 2.19 (0.61–7.88) .229

note. The variables incorporated in the final model for prevalence on hands were hospital, occupation, and sex (for gram-negative bacteria); hospitaland unit (for Enterobacteriaceae); and hospital (for nonfermentative gram-negative bacteria). The variables incorporated in the final model for transmissionto investigators hand were hospital (for gram-negative bacteria and nonfermentative gram-negative bacteria). CI, confidence interval; ND, not determined(because of low incidence); OR, odds ratio.

analysis of covariance of natural logarithm–transformed data,controlling for potential confounding variables, revealed nosignificant influence of rings alone (Table 2).

For all hand contacts combined (irrespective of rings), asignificant correlation was detected between the bacterialloads on hands and the bacterial load transferred during stan-dardized hand contact ( , Pearson’s r coefficient). TheP ! .001median bacterial load on the gloved hands of the investigatorsafter hand contact ( ) was 1,500 CFU (range, 0–n p 400358,000 CFU). Significantly higher numbers of bacteria weretransmitted from the hands of HCWs with rings than fromthe hands of HCWs without rings (Table 1). However, similarto the case of bacterial load on hands, multivariate analysisrevealed no significant effect of rings alone on transmission(Table 2).

S. aureus

S. aureus was recovered from 71 (17.8%) of 400 hands of 52(26.0%) of the 200 HCWs. Twenty-one participants (21.0%)who wore rings and 31 participants (31.0%) who did notwear rings had S. aureus on 1 or both hands. The differencewas not statistically significant by using nonpaired analysiscomparing ringed hands with a randomly selected hand fromeach participant in the control group (adjusting for handdominance; , Pearson x2 test) or by using pairedP p .212analysis (same person; , McNemar x2 test).P 1 .99

S. aureus was detected on 27 (6.8%) of 400 gloved hands.In the subgroup of 52 HCWs with S. aureus on 1 or bothhands, transmission to 1 or both gloved hands after handcontact was detected in 22 cases (42.3%). No statisticallysignificant differences were found between transmission of S.aureus from ringed and nonringed HCWs by using nonpairedanalysis comparing ringed hands with a randomly selectedhand from each HCW in the control group (adjusting forhand dominance; 9 [9.0%] vs 9 [9.0%]; , by the Pear-P 1 .99son x2 test) or by using paired analysis (same person; datanot shown).

Gram-Negative Bacteria

One or more species of gram-negative bacteria was recoveredfrom 167 (41.8%) of the 400 hand samples from 110 (55.0%)

of the 200 HCWs. Enterobacteriaceae were recovered from79 (19.8%) of the hands and 57 (28.5%) of the participants,and nonfermentative gram-negative bacteria were recoveredfrom 130 (32.5%) of the hands and 95 (47.5%) of the par-ticipants. In the comparison of ringed hands with a randomlyselected hand from each participant in the control group(adjusting for hand dominance), significantly higher preva-lences of nonfermentative gram-negative bacteria (42 [42.0%]vs 26 [26.0%]) and Enterobacteriaceae (26 [26%.0] vs 13[13.0%]) were found among participants who wore rings thanamong control subjects (Table 3). No statistically significantdifferences in the prevalence of nonfermentative gram-neg-ative bacteria or Enterobacteriaceae were found between theringed hands and the hands without rings in the group withrings (data not shown).

One or more gram-negative bacterial species was detectedon 27 (6.8%) of 400 gloved hands. Twelve contacts (3.0%)resulted in transmission of Enterobacteriaceae, and 21 (5.3%)resulted in transmission of nonfermentative gram-negativebacteria. In the comparison of transmission from ringedhands with transmission from a randomly selected hand fromeach participant in the control group (adjusting for handdominance), no statistically significant differences in the in-cidence of transmission of gram-negative bacteria (16% vs9%), Enterobacteriaceae (3% vs 2%), or nonfermentativegram-negative bacteria (9% vs 4%) were detected by using



finger rings and transmission of bacteria 431

nonpaired analysis (Table 3) or by using paired analysis (sameperson; data not shown).

discussion

The main objective of the present study was to examine theimpact of finger rings on bacterial transmission from natu-rally contaminated hands. To our knowledge, no such studyhas been previously reported. In addition, we aimed to repeatour previous study of the impact of finger rings on the mi-croflora on the hands of HCWs. To mimic what we considerto be the most frequent mode of contact in clinical care, adry gloved hand was used as the recipient surface, with ap-plication of moderate friction for approximately 30 seconds.16

The overall results regarding total bacterial load and prev-alence of S. aureus and gram-negative bacteria on the handsof HCWs were similar to those from other studies that usedthe glove juice method.18-26 We found a significant correlationbetween the total bacterial load on HCW hands and the bac-terial load transmitted to investigator hands. Furthermore,we detected significantly higher bacterial loads on ringedhands than on hands of control subjects; these results are incontrast to our previous study that involved plain rings only.1

We also measured a significantly higher number of bacteriatransmitted during contacts with ringed hands, comparedwith contacts with hands of the control subjects. However,an analysis of covariance of natural logarithm–transformeddata (controlling for potential confounding variables) re-vealed no statistically significant effect of rings alone on bac-terial load on HCW hands or on the bacterial load transmittedto investigator hands.

In the present study, significantly higher prevalences ofboth Enterobacteriaceae and nonfermentative gram-negativebacteria were found on the hands of participants who worerings, even after controlling for potential confounding vari-ables. The same observation was made in our previous studyfor Enterobacteriacea but not for nonfermentative gram-neg-ative bacteria.1 However, despite the increased prevalence ofthese species on the hands of HCWs with rings, no statisticallysignificant differences in the incidence of transmission weredetected between the group with rings and the group withoutrings. This may be attributable to a low degree of transmissionunder the circumstances tested. We have recently reported avery low incidence of transmission from hands artificiallycontaminated with Escherichia coli.16 A small gram-negativebacterial load per HCW hand may also have contributed toa low rate of transmission. In the present study, we did notprecisely quantify gram-negative bacteria, but semiquanti-tative estimates indicated that, in most cases, only a few thou-sand gram-negative bacteria were recovered from the donorhands. Exact quantification of gram-negative bacteria and S.aureus and a larger number of HCWs included in the studymight have resulted in a statistically significant influence onthe incidence of transmission. We argue, however, that theclinical relevance would be minor for this type of contact. In

situations with more extensive hand contamination, however,the results may be different.

This study has several limitations. First, because our studyinvolved naturally contaminated hands, we were not able todiscriminate between permanent microflora and transientcontamination, even though our results with S. aureus andgram-negative bacteria may be indicative of transient con-tamination. Transient bacteria may be expected to detachmore easily from hands and will probably more frequentlybe potentially pathogenic, compared with bacteria belongingto the permanent flora. The clinical consequences of trans-mission of even small numbers of transient bacterial isolatesmay therefore potentially be more serious.

Second, the results are not valid for wet contacts27-29 orcontacts involving more extensive friction30 or longer dura-tion. Such contacts may be expected to result in more ex-tensive transmission. Even though these types of contacts aresupposedly less frequent than the contact mode simulated inthe present study, one such contact may be sufficient to resultin transmission.

Third, the study was designed to examine the impact offinger rings on bacterial load and transmission from hands,controlling for a number of potential confounders. Severalof these confounders influenced the results, and they have tobe further studied.

acknowledgments

We thank Tone Herring, Anne Ottestad Syvertsen, Terje Lingaas, and TrondLingaas, for technical assistance, Magne Thoresen, for advice on statisticalanalysis, and May-Solveig Fagermoen, for valuable comments in the intro-ductory part of this study.

Financial support. Helse Sør RHF, Norway.Potential conflicts of interest. M.F. and E.L. report no conflicts of interest

relevant to this article.

Address reprints request to Mette Fagernes, Sykehuset i Vestfold, KlinikkMedisin, Postboks 2168, Postterminalen, N-3103 Tønsberg, Norway ([email protected]).

Presented in part: 18th Annual Scientific Meeting of the Society for Health-care Epidemiology of America; Orlando, Florida; April 2008 (Abstract 511).

references

1. Fagernes M, Lingaas E, Bjark P. Impact of a single plain finger ring onthe bacterial load on the hands of healthcare workers. Infect Control HospEpidemiol 2007; 28:1191-1195.

2. Nicholson-Pegg A. The wearing of wedding rings in the operating de-partment. NATNEWS 1982; 19:19-25.

3. Hoffman PN, Cooke EM, McCarville MR, Emmerson AM. Micro-or-ganisms isolated from skin under wedding rings worn by hospital staff.Br Med J (Clin Res Ed) 1985; 290:206-207.

4. Jacobson G, Thiele JE, McCune JH, Farrell LD. Handwashing: ring-wearing and number of microorganisms. Nurs Res 1985; 34:186-188.

5. Salisbury DM, Hutfilz P, Treen LM, Bollin GE, Gautam S. The effect ofrings on microbial load of health care workers’ hands. Am J Infect Control1997; 25:24-27.

6. Trick WE, Vernon MO, Hayes RA, et al. Impact of ring wearing on hand




contamination and comparison of hand hygiene agents in a hospital.Clin Infect Dis 2003; 36:1383-1390.

7. Alp E, Haverkate D, Voss A. Hand hygiene among laboratory workers.Infect Control Hosp Epidemiol 2006; 27:978-980.

8. Kelsall NK, Griggs RK, Bowker KE, Bannister GC. Should finger ringsbe removed prior to scrubbing for theatre? J Hosp Infect 2006; 62:450-452.

9. Jepson AP, McDougall C, Clark A, Bateman A, Williamson G, KaufmannME. Finger rings should be removed prior to scrubbing. J Hosp Infect2006; 64:197-198.

10. Yildirim I, Ceyhan M, Cengiz AB, et al. A prospective comparative studyof the relationship between different types of ring and microbial handcolonization among pediatric intensive care unit nurses. Int J Nurs Stud2008;45:1572-1576.

11. Athar MA, Stafford L, Wootliff JS. Bacterial population of ring andcontrol fingers in health care workers. Infect Control Can 1989;8-12.

12. Field EA, McGowan P, Pearce PK, Martin MV. Rings and watches: shouldthey be removed prior to operative dental procedures? J Dent 1996; 24:65-69.

13. Al-Allak A, Sarasin S, Key S, Morris-Stiff G. Wedding rings are not asignificant source of bacterial contamination following surgical scrub-bing. Ann R Coll Surg Engl 2008; 90:133-135.

14. Aiello AE, Cimiotti J, la-Latta P, Larson EL. A comparison of the bacteriafound on the hands of “homemakers” and neonatal intensive care unitnurses. J Hosp Infect 2003; 54:310-315.

15. Waterman TR, Smeak DD, Kowalski J, Hade EM. Comparison of bac-terial counts in glove juice of surgeons wearing smooth band rings versusthose without rings. Am J Infect Control 2006; 34:421-425.

16. Lingaas E, Fagernes M. Development of a method to measure bacterialtransfer during hand contact. J Hosp Infect 2009 (Epub ahead of print).

17. European Committee for Standardization. Chemical disinfectants andantiseptics—hygienic handwash—test methods and requirements. Phase2. Step 2. Brussels: European Committee for Standardization, 1997.

18. Larson EL, Laughon BE. Comparison of four antiseptic products con-taining chlorhexidine gluconate. Antimicrob Agents Chemother 1987; 31:1572-1574.

19. Gustafson DR, Vetter EA, Larson DR, et al. Effects of 4 hand-dryingmethods for removing bacteria from washed hands: a randomized trial.Mayo Clin Proc 2000; 75:705-708.

20. Kampf G, Ostermeyer C, Heeg P, Paulson D. Evaluation of two methodsof determining the efficacies of two alcohol-based hand rubs for surgicalhand antisepsis. Appl Environ Microbiol 2006; 72:3856-3861.

21. Larson E, Aiello A, Lee LV, la-Latta P, Gomez-Duarte C, Lin S. Short-and long-term effects of handwashing with antimicrobial or plain soapin the community. J Community Health 2003; 28:139-150.

22. McBryde ES, Bradley LC, Whitby M, McElwain DL. An investigation ofcontact transmission of methicillin-resistant Staphylococcus aureus. J HospInfect 2004; 58:104-108.

23. Waters V, Larson E, Wu F, et al. Molecular epidemiology of gram-negativebacilli from infected neonates and health care workers’ hands in neonatalintensive care units. Clin Infect Dis 2004; 38:1682-1687.

24. Horn WA, Larson EL, McGinley KJ, Leyden JJ. Microbial flora on thehands of health care personnel: differences in composition and antibac-terial resistance. Infect Control Hosp Epidemiol 1988; 9:189-193.

25. Larson EL. Persistent carriage of gram-negative bacteria on hands. AmJ Infect Control 1981; 9:112-119.

26. Petersen NJ, Collins DE, Marshall JH. Evaluation of skin cleansing pro-cedures using the wipe-rinse technique. Health Lab Sci 1974; 11:182-187.

27. Marples RR, Towers AG. A laboratory model for the investigation ofcontact transfer of micro-organisms. J Hyg (Lond) 1979; 82:237-248.

28. Patrick DR, Findon G, Miller TE. Residual moisture determines the levelof touch-contact-associated bacterial transfer following hand washing.Epidemiol Infect 1997; 119:319-325.

29. Merry AF, Miller TE, Findon G, Webster CS, Neff SP. Touch contami-nation levels during anaesthetic procedures and their relationship to handhygiene procedures: a clinical audit. Br J Anaesth 2001; 87:291-294.

30. Sattar SA, Springthorpe S, Mani S, et al. Transfer of bacteria from fabricsto hands and other fabrics: development and application of a quantitativemethod using Staphylococcus aureus as a model. J Appl Microbiol 2001; 90:962-970.



impact of finger rings on transmission of bacteria during hand contact •

Documents