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

JAN JOURNAL OF ADVANCED NURSING

ORIGINAL RESEARCH

Factors interfering with the microflora on hands: a regression analysis of
samples from 465 healthcare workers
Mette Fagernes & Egil Lingaas

Accepted for publication 13 August 2010

Correspondence 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 on
e-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.x
Mette Fagernes RN
PhD Student
Department of Internal Medicine, Vestfold
Abstract
Hospital 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 hand
University of Oslo, Norway microbiology of healthcare workers.
Background. The impact of the above mentioned variables on hand microbiology
Egil 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 the
Rikshospitalet University Hospital, Oslo,
glove juice method during two study periods (2004 and 2007), and examined for total
Norway
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 healthcare
Introduction
workers (HCWs). Consequently, hand hygiene is regarded
Health care associated infections (HAI) are major sources of as one of the most fundamental infection prevention
morbidity 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

M. Fagernes and E. Lingaas

Background People were excluded if they had skin irritation or eczema,
if they had taken antibiotics during the previous 2 weeks or
Many 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 were
regard 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 (only
occupation (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 since
contradictory. There is a lack of studies suitable for multi-
most recent hand washing, hand disinfection and use of hand
variate analysis, which is a drawback since many of these
lotion, and time since most recent glove use if hand hygiene
variables 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 differing
recommendations on these issues in current guidelines on Data collection and microbial methods
hand hygiene (Larson 1995, Boyce & Pittet 2002, Pratt et al.
The data were collected during two separate study periods in
2007, World Health Organization 2009). We therefore need
2004 and 2007 (Fagernes et al. 2007, Fagernes & Lingaas
more data to substantiate the role of these variables in order
2009). Both hands were sampled with a modified version of
to 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 with
The study
neutralizer as previously described (Fagernes et al. 2007,
Fagernes & Lingaas 2009). The bag was occluded around the
Aims
wrist, and the hand was massaged in a standardized manner
The aim of the present study was to determine the impact of by an investigator for approximately 1 minute. The sampling
the above mentioned variables in a large cohort of HCWs and fluid was collected in a sterile container and total bacterial
in ordinary clinical settings by the use of multivariate counts were measured according to the European Norm 1499
analysis. (European Committee for Standardization 1997). Staphylo-
coccus aureus, Enterobacteriacea and non-fermentative
Gram-negative rods (NFGNR) were identified to the species
Study design
level, but were not quantified. The theoretical sensitivity for
We used a cross-sectional design, appropriate for collecting detection of S. aureus was 500 CFU per hand in study period
empiric 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 1–58
Participants
and 10 CFU per hand for subject 59–200.
A convenience sample of 465 HCWs directly involved in
patient care (i.e. physicians, nurses, assistants, phlebotomists,
Ethical considerations
physiotherapists and radiography personnel) from three Nor-
wegian acute care hospitals were recruited into the study, 265 Participation was voluntary and the HCWs were given oral
in study period 1 (2004) and 200 in study period 2 (2007). and written information before consenting to participate. The
They were interrupted between ordinary clinical work activ- studies were approved by the institutional review board at all
ities 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 at
random days. No notification was give in advance, and no
Data analysis
extra hand hygiene was allowed before the hand samples were
taken. HCWs were collected based on the aim to include The median of the average number of bacteria on both hands
approximately the same numbers with and without rings. of each HCW and the presence of S. aureus, Enterobacteri-

298 Ó 2010 Blackwell Publishing Ltd

JAN: ORIGINAL RESEARCH Variables having an impact on hand contamination

aceae and NFGNR on one or both hands were used as Table 1 Study participants and study variables
outcome variables.
First study Second study
To account for the positive skewness of the measured data, period period Total
log-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 Gender
analyses 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
Occupation
one 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)
personnel
ical 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 Shift
a 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 sampling
residuals, 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 watch
method 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 disinfection



Table 1 (Continued) final regression model were hand disinfection, nail length,
nail polish and hospital.
First study Second study
period period Total
Variable (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 75
Minutes 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 number
Values are given as n (%).
were found to influence the occurrence of NFGNR. Table 4
and 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: OR
strated significantly higher total bacterial counts than on 2Æ21 (95% CI: 1Æ21–4Æ03), P = 0Æ010] which disappeared
control hands [unadjusted effect estimate: 5Æ70 (95% CI: after adjusting for finger rings and nail polish in the final
3Æ04–10Æ68), 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 effect
Variable (95% CI) P value (95% CI) P value

Finger 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) 0Æ001
Minutes 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) 0Æ020
Study period – <0Æ001 – <0Æ001
Study 1 (2004) Reference group – Reference group –
Study 2 (2007) 0Æ29 (0Æ21–0Æ39) <0Æ001 0Æ32 (0Æ23–0Æ43) <0Æ001



Table 3 Multivariate logistic regression analysis of variables with an impact on the occurrence of Enterobacteriaceae on the hands of
healthcare workers (N = 465)

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

Hospital – <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) 0Æ001
Occupation – 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) 0Æ207
Finger 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) 0Æ133
Study period – <0Æ001 – 0Æ001
Study 2 (2007) 5Æ47 (3Æ10–9Æ70) <0Æ001 3Æ52 (1Æ68–7Æ39) 0Æ001

Table 4 Multivariate logistic regression analysis of variables with an impact on the occurrence of non-fermentative Gram-negative rods on the
hands of healthcare workers (N = 465)

Adjusted OR

Hospital – <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) <0Æ001
Minutes since hand – 0Æ127 – 0Æ021
disinfection
<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) 0Æ657
Study period – <0Æ001 – 0Æ092
Study 2 (2007) 2Æ57 (1Æ74–3Æ80) <0Æ001 1Æ61 (0Æ93–2Æ78) 0Æ092

Staphylococcus aureus Discussion
Staphylococcus aureus was detected on one or both hands of
Study limitations
120 (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 465
application 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 different
multivariate analysis. Table 5 describes effect estimates for units were visited at random days. The results are expected to
the variables in the ﬁnal model. be generalizable across international hospital settings, but



Table 5 Multivariate logistic regression analysis of variables with an impact on the occurrence of Staphylococcus aureus on the hands of
healthcare workers (N = 459)

Adjusted OR

Occupation – 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) 0Æ056
Length 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) 0Æ518
Minutes since use of – 0Æ009 – 0Æ006
hand lotion
<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) 0Æ247
Study period – 0Æ934 – 0Æ072
Study 2 (2007) 1Æ02 (0Æ67–1Æ55) 0Æ934 1Æ54 (0Æ96–2Æ46) 0Æ072

potential differences were not explored. It is not known to studies comparing hand microflora of different healthcare
which 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 nurses
Gender
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 12
bacterial 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 bacterial
microflora 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 HCWs
40 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 fingernails
was not statistically significant (P = 0Æ156).
Multivariate analysis demonstrated a statistically significant
correlation between fingernails longer than 2 mm and
Occupation
prevalence of S. aureus, but no association with carriage
Using nurses as reference, nursing assistants had higher of Gram negative rods or total bacterial numbers. We have
carriage rate of S. aureus, whereas the prevalence was lower identified two published studies on the influence of the
among radiography personnel. The latter group, however, length of natural nails. Rupp et al. (2008) examined 192
more frequently carried Enterobacteriaceae. No differences samples from the dominant hand of 69 nurses over a 2-year
were found in total bacterial counts between nurses and other period and found increased bacterial counts with nail length
occupational groups. We have identified four published above 2 mm, but no difference in the recovery of Gram



negative 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 bacteria
the 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 the
Neither of these two studies reported the prevalence of bacterial load on finger tips when the watch was kept in
S. 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 of
guidelines 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 as
Control and Prevention (CDC) (Boyce & Pittet 2002) and the many bacteria from hands with watches compared to control
World Health Organization (WHO) (World Health Organi- hands. We recommend that HCW abstain from the use of
zation 2009) recommend nail length less than 1/4-inch wrist watches at work.
(6Æ3 mm), and 5 mm respectively. Based on the findings of
the present study and the results of Rupp et al. (2008), we
Finger rings
recommend that the fingernails of HCWs should not be
longer 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 for
Nail polish
watches in the aggregated 2004/2007 data. Watches were
No impact of nail polish was detected in this study. We are not shown to significantly increase bacterial numbers in the 2007
aware of any other study examining the impact of nail polish study, which also demonstrated a significant correlation
on the microflora of the whole hand. Three studies, sampling between the use of rings and watches; 64% of ring wearers
the nails only, did not show any influence of polish on used a wrist watch compared to 15% of the HCW without
bacterial 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 prevalence
studies with 100 and 61 participants respectively demon- was revealed for one plain ring only. We assume that the
strated 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 a
pants with nail polish on one hand only (Baumgardner et al. single plain ring and no ring. No influence of rings was
1993). 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 of
polish. 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). Most
of 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, and
while the English guideline state that wrist jewellery should an increased prevalence of Gram negative bacteria. Results
be removed prior to patient contact (Pratt et al. 2007). Only from studies of the association between rings and hand
two studies have previously been published on this issue. contamination after hand hygiene are less consistent. In
Field et al. (1996) found that skin below wrist watches particular, several studies failed to show differences after
harbours more bacteria than control skin on the opposite surgical hand antisepsis (Jacobson et al. 1985, Waterman
wrist. Jeans et al. (2010) investigated the impact of wrist et al. 2006, Wongworawat & Jones 2007).



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 all
about wearing rings in healthcare settings, and that this is an 5-minute intervals after disinfection, except for samples
unresolved 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 group
accept 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 has
Organization 2009). UK guidelines issued in 2007 state that a biphasic effect on hand microflora with an initial reversible
all 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 a
support this recommendation. reduced prevalence of NFGNR. This is probably due to a



sustained effect on the permanent skin flora, which frequently
Funding
contains 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 Sør
tatives 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 hands
in 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 periods

We found significantly lower bacterial load on hands in the
Author contributions
second study period. This can probably be explained by a
significant increase in the use of alcoholic hand disinfection MF and EL were responsible for the study conception and
from the first to the second study period. Also, a significantly design. MF performed the data collection. MF performed the
higher prevalence of Gram negative bacteria was observed, data analysis. MF and EL were responsible for the drafting of
which may be a result of enhanced sensitivity of the detection the manuscript. MF and EL made critical revisions to the
method. These differences are taken into consideration in the paper for important intellectual content. MF provided
regression analysis by including study period as an indepen- statistical expertise. MF obtained funding. MF and EL
dent variable. provided administrative, technical or material support. EL
supervised the study.

Conclusion
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