JAC-

Antimicrobial
Resistance
JAC Antimicrob Resist
https://doi.org/10.1093/jacamr/dlac051

Hand and nasal carriage of Staphylococcus aureus and its rate

of recolonization among healthcare workers of a tertiary care
hospital in Nepal
Junu Richhinbung Rai1, Ritu Amatya1* and Shiba Kumar Rai1

1
Department of Microbiology, Nepal Medical College, Kathmandu, Nepal

*Corresponding author. E-mail: [email protected]

Received 5 March 2022; accepted 28 April 2022

Background: Carriers of Staphylococcus aureus among healthcare workers (HCWs) can spread the bacteria to
patients and the environment, in addition to their own risk of infection.
Objectives: To determine the prevalence of S. aureus carriers among HCWs and the rate of recolonization after
decolonization therapy with mupirocin.
Methods: Nasal and hand swabs from HCWs of a tertiary care hospital in Nepal were cultured on mannitol salt
agar and S. aureus isolated were identified using standard microbiological procedures. Detection of MRSA and
mupirocin-resistant S. aureus (MupRSA) isolates were done phenotypically. Identified S. aureus carriers were de-
colonized with 2% mupirocin nasal ointment. Recolonization of the carriers was assessed monthly for the next
5 months.
Results: Among the 213 HCWs, 18.3% were S. aureus carriers (35 nasal carriers, 4 both nasal and hand carriers,
and no hand carriers). Overall, 9.4% of the HCWS were MRSA carriers and none were MupRSA carriers. After de-
colonization, 25.6% of them were recolonized and 50.0% of the recolonization was detected after 3 months of
decolonization. All recolonized carriers had only MSSA strains (which colonized only nose), and none were reco-
lonized with MupRSA.
Conclusions: HCWs are frequent carriers of S. aureus and MRSA. Due to their continuous exposure to the hospital
environment, they are at risk of colonization by this MDR organism. Regular screening and decolonization of
HCWs working with high risk, vulnerable patients would reduce the risk of MRSA transmission from HCWs to
patients.

Introduction subsequent S. aureus infection and are presumed to be an im-

portant source of MRSA.1,5 Mupirocin, a mixture of many pseudo-
Healthcare workers (HCWs) harbouring pathogens are an import- monic acids that can bind to the isoleucine-specific binding
ant reservoir of pathogens responsible for hospital-acquired in- pocket of the bacterial isoleucyl-tRNA synthetase (IleRS), is re-
fection (HAI) and are considered the interface between the commended as a potent decolonizing agent in the carrier
healthcare centres and the community.1 Staphylococcus aureus, HCWs.6,7 However, there have been reports of increasing mupiro-
a common pathogen of HAI, causes infections ranging from min- cin resistance.8
or localized infections to fatal systemic infections, that have se-
vere consequences, even with antimicrobial therapy.2,3 This
Materials and methods
pathogen is also a commensal of the skin and nasal mucosa.2
Nasal and hand carriage of the bacteria are strongly correlated Ethics
as hands are the main vector for transmitting the pathogen be- The ethical clearance for this study was obtained from the Institutional
tween the nose-picking area (anterior nares) and the surfaces.2,4 Research/Ethical Review Committee (RERC) of Nepal Medical College in
Asymptomatic nasal carriers among HCWs are at a high risk of Kathmandu, Nepal.

© The Author(s) 2022. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://
creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided
the original work is properly cited. For commercial re-use, please contact [email protected]
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Rai et al.

Methods The 39 S. aureus carriers were decolonized with 2% mupirocin

Nasal and hand swabs were collected using commercially available nasal ointment. The decolonization therapy was 100% success-
sterile non-absorbent cotton swabs from HCWs of six departments of a ful, as proven by no detection of S. aureus in all carriers after a
tertiary care centre in Nepal. Those who gave informed consent and month of decolonization. Recolonization was detected in 10
who had not used mupirocin ointment nasally or had a chlorhexidine (25.6%) of the 39 carriers and the highest recolonization was
bath in the last 1 month were included in the study. Required details after 3 months of decolonization followed by 4 months and
were obtained using questionnaires. For nasal swab, the swab was in- 2 months. Ten (28.6%) of the 35 nasal carriers were recolonized
serted 2–3 cm into the anterior nares and rotated four times both clock- while none (0/4) of those who were both nasal and hand carriers
wise and anticlockwise before withdrawal. For hand swab, the web-space were recolonized (P . 0.05).
of the hand was swabbed with sterile cotton swab moistened in sterile
The rate of recolonization was slightly more in MSSA carriers
brain heart infusion (BHI) broth. Swabs were immediately inoculated on
than MRSA carriers (P . 0.05). All 10 were recolonized with
mannitol salt agar (MSA) and incubated at 37°C. Yellow distinct colonies
on MSA were presumed to be colonies of S. aureus and subcultured on nu- MSSA. Additionally, none of the recolonized carriers were
trient agar (NA). Golden yellow colonies on NA that were Gram-positive MupRSA carriers. Recolonization was seen more among the car-
cocci in clusters, producing catalase and coagulase were identified as riers with the habit of nose-picking than those without this habit
S. aureus. All confirmed S. aureus isolates were tested for detection of (P .0.05). Interestingly, the carriers who followed the WHO
methicillin and mupirocin resistance by Kirby–Bauer disc diffusion and in- guideline of hand washing had more recolonization than those
terpreted as per CLSI 2017 guidelines9 and Kaur and Narayan.10 All iden- who did not (P . 0.05). All recolonized carriers were only nasal
tified carriers were decolonized with 2% mupirocin nasal ointment carriers. Females had a higher rate of recolonization than males
bilateral application twice a day for 5 days. Nasal and hand swabs were (P . 0.05). Recolonization was highest among carriers in
collected from all carriers on a monthly basis five times. All swabs were
the age group of 20–29 years while none in the age group of
subjected to identification of S. aureus, MRSA and mupirocin-resistant
40–49 years were recolonized.
S. aureus (MupRSA).
The highest rate of recolonization was seen in the Paediatrics
(including PICU and NICU) and Surgery departments, followed
Statistical analysis by the Obstetrics and Gynaecology, Neurosurgery, Clinical
Laboratory and Medicine departments. Overall, recolonization
All the data were recorded and analysed using International Business
was highest among doctors (42.9%), followed by nurses
Machine Statistical Package for the Social Sciences (IBM SPSS) version
19. χ2 test was used to analyse the results and P value , 0.05 was con- (35.3%), attendants (8.3%) and laboratory personnel (0.0%)
sidered statistically significant. but this was statistically not significant using Pearson’s χ2 test.
Females had a higher recolonization rate in all departments,
except in the surgical department where recolonization was
equal among males and females, although this finding was stat-
Results
istically not significant. As shown in Table 2, the highest rate of
Among the total 213 HCWs included in the study, 39 (18.3%) recolonization was among doctors in Surgery, Obstetrics and
were identified as S. aureus carriers. The prevalence was higher Gynaecology and Clinical Laboratory departments, nurses in
among the females (22.8%) compared to the males (12.2%) Neurosurgery and Medicine departments and both nurses and
(P , 0.05). Table 1 shows that majority of the carriers were from attendants had an equal rate of recolonization in Paediatrics (in-
the Obstetrics and Gynaecology Department, followed by cluding PICU and NICU) department (P . 0.05).
Neurosurgery, Surgery (general surgery, gastrointestinal surgery
and urosurgery), Medicine, Clinical Laboratory and Paediatrics,
Discussion
including paediatric ICU (PICU) and neonatal ICU (NICU).
Attendants had the highest prevalence followed by nurses, The carrier status of S. aureus among HCWs in this study, i.e.
laboratory personnel and doctors. All participants were adults 18.3%, is exactly the same as reported in 2017 from Nepal by
(lowest age of 22 years; highest age of 45 years) and there Khatri et al.11 The present finding was also comparable to other
were more S. aureus carriers as well as MRSA carriers among reports from Nepal by Khanal et al. (15.7%),12 Sah et al.
HCWs in the age group of 40–49 years. (20.4%)13 and Mukhiya et al. (20.9%).14 On the contrary, Pant
The association of the habit of nose-picking with S. aureus car- and Rai15 reported a significantly higher prevalence of 51.9%
riage was statistically significant with OR of 14.6 (95% CI = 6.485 among the HCWs of the same tertiary care in 2007. This reduction
to 32.725) using Pearson’s χ2 test. There were more carriers in prevalence could be due to increased awareness and
among the HCWs who did not follow the WHO guideline of implementation of infection control measures during recent
hand washing than those who followed the guideline. This finding years. The present finding was lower than those reported from
was statistically significant using Pearson’s χ2 test with OR of Nepal (27.3% to 92.0%),16–18 India (22.2% to 48.0%),3,10,19,20
0.376 (95% CI = 0.185 to 0.764). Among the 39 carriers, 13 had Northeast Ethiopia (28.8%),21 Iran (31.0%)22 and Israel
the habit of nose-picking as well as did not follow the WHO guide- (31.0%).23 However, lower prevalence of 7.7% to 15.6% has
line of hand washing, 12 followed the WHO guideline of hand also been reported.24–26
washing but had the habit of nose-picking, 10 had no habit of S. aureus was detected more from the anterior nares than the
nose-picking but did not follow the WHO guideline of hand wash- hands in this study, which is similar to the report of Pant and
ing, and 4 had no habit of nose-picking and also followed the Sharma.18 This finding corresponds to the fact that anterior nares
WHO guideline of hand washing. Out of the total 213 HCWs, are the most common site of S. aureus colonization. Reports of
20 (9.4%) were MRSA carriers and none were MupRSA carriers. hand carriers are limited in comparison to the nasal carriers.

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Table 1. Prevalence of S. aureus carriers and MRSA carriers among different types of HCWs in each department

Department Profession Total S. aureus carriers (%) P value MRSA carriers (%) P value

Obstetrics and Gynaecology Doctor 10 1 (10.0) 0.2 0 (0.0) 0.7

Nurse 11 5 (45.5) 2 (18.2)
Attendant 4 2 (50.0) 1 (25.0)
Total 25 8 (32.0) 3 (12.0)
Neurosurgery Doctor 6 1 (16.7) 0.2 0 (0.0) 0.5
Nurse 8 1 (12.5) 0 (0.0)
Attendant 3 2 (66.7) 1 (33.3)
Total 17 4 (23.5) 1 (5.9)
Surgery Doctor 9 1 (11.1) 0.1 1 (11.1) 0.3
Nurse 15 3 (20.0) 3 (20.0)
Attendant 3 2 (66.7) 1 (33.3)
Total 27 6 (22.2) 5 (18.5)
Medicine Doctor 21 2 (9.5) 0.2 1 (4.8) 0.3
Nurse 26 6 (23.1) 2 (7.7)
Attendant 5 2 (40.0) 2 (40.0)
Total 52 10 (19.2) 5 (9.6)
Clinical Laboratory Doctor 14 2 (14.3) 0.7 0 (0.0) 0.3
Laboratory personnel 24 3 (12.5) 2 (8.3)
Attendant 8 2 (25.5) 1 (12.5)
Total 46 7 (15.2) 3 (6.5)
Paediatrics (including PICU and NICU) Doctor 12 0 (0.0) 0.1 0 (0.0) 0.2
Nurse 27 2 (7.4) 2 (7.4)
Attendant 7 2 (28.6) 1 (14.3)
Total 46 4 (8.7) 3 (6.5)

The prevalence of hand carriers in this study was lower than those been due to lesser awareness of hygiene maintenance and infec-
reported by Mukhiya et al.14 and Pant and Sharma,18 which could tion control practices.
indicate better hand hygiene among the participating HCWs in this The majority of the HCWs with the habit of nose-picking were
study. All four hand carriers in this study were also nasal carriers identified as carriers. This habit transmits S. aureus from contami-
and the isolates from both sites had the same antibiogram, sug- nated surfaces to the nasal niche, and vice versa.2 HCWs follow-
gesting them to be of same clone phenotypically. Additionally, ing the WHO guideline of handwashing had a lower carrier rate
these carriers had the habit of nose-picking, which supports the than those who did not. Appropriate hand hygiene practices
fact of hands being the main vector in dissemination of S. aureus among HCWs is effective in MRSA control.27 However, these
from surfaces to the anterior nares and vice versa. Other informa- data were obtained from questionnaires and may be biased.
tion of S. aureus dissemination to external environment and vice In this study, there were 9.4% MRSA carriers among a total of
versa (such as mere contact with anterior nares) and identification 213 HCWs, which is more than other reports from Nepal: 5.7% in
of throat carriers were not assessed in this study. 2007 (from the same study area), 2.3% in 2009 from another ter-
While there are reports of more female carriers than males tiary care centre in Nepal,16 3.4% in 2015 from western Nepal,12
similar to this study,10,13,17 many reports show male preponder- 6.3% in 2015 from Iran,25 3.3% in 2015 from India.26 The global
ance too.2–4,11,12,21 On the contrary, Askarian et al.22 reported no rise in antimicrobial-resistant strains, especially in hospital set-
significant difference between males and females in their study tings, could be the reason behind this. But the present finding
among HCWs of Iran. was lower than the 25.0% reported by Shakya et al.17 from west-
The Obstetrics and Gynaecology department had the highest ern Nepal in 2010, 12.5% from India in 201619 and 12.7% from
rate of carriers, which does not correspond to the other reports of Northeast Ethiopia in 2014,21 which could be due to differences
highest findings in Orthopaedics,3 in Medicine23 and in the in implementation of infection control practices.
Post-operative Ward.11 In this study, the Paediatrics department The in vitro finding of no MupRSA carriers was further con-
(including PICU and NICU) had the lowest prevalence of carriers, firmed by effective decolonization of all the carriers by 2% mupir-
which could be due to stricter implementation of masks and ocin ointment. In contrast, there are reports of MupRSA carriers
hand hygiene protocols by HCWs during patient care. However, among 31.4% of S. aureus carriers from India in 2016,19 7.0%
there are other reports of the highest rate of carriers in the among MRSA carriers by Agarwal et al. from India in 2015,20
Paediatrics department and in the ICU.13,21 and 1.4% among MRSA carriers by Kaur and Narayan from
Similar to the finding in this study, Kaur and Narayan10 also re- India in 2014.10
ported the lowest prevalence of carriers among the doctors. The Ten (25.6%) of the 39 carriers were recolonized after decolon-
highest prevalence among attendants in this study could have ization in this study, which is comparable to the finding (24.0%) of

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Table 2. Rate of S. aureus recolonization among different types of HCW from each department

Department Profession S. aureus carriers Recolonized carriers % P value

Paediatrics (including PICU and NICU) Doctor (n = 12) 0 0 0.0 1.000

Nurse (n = 27) 2 1 50.0
Attendant (n = 7) 2 1 50.0
Total (n = 46) 4 2 50.0
Surgery Doctor (n = 9) 1 1 100.0 0.189
Nurse (n = 15) 3 2 66.7
Attendant (n = 3) 2 0 0.0
Total (n = 27) 6 3 50.0
Obstetrics and Gynaecology Doctor (n = 10) 1 1 100.0 0.155
Nurse (n = 11) 5 1 20.0
Attendant (n = 4) 2 0 0.0
Total (n = 25) 8 2 25.0
Neurosurgery Doctor (n = 6) 1 0 0.0 0.135
Nurse (n = 8) 1 1 100.0
Attendant (n = 3) 2 0 0.0
Total (n = 17) 4 1 25.0
Clinical Laboratory Doctor (n = 14) 2 1 50.0 0.233
Lab personnel (n = 24) 3 0 0.0
Attendant (n = 8) 2 0 0.0
Total (n = 46) 7 1 14.3
Medicine Doctor (n = 21) 2 0 0.0 0.690
Nurse (n = 26) 6 1 16.7
Attendant (n = 5) 2 0 0.0
Total (n = 52) 10 1 10.0

Watanakunakorn et al.28 All recolonized carriers were nasal car- but also the possibility of recolonization even after successful de-
riers, which supports the statement that the anterior nares are colonization. Routine screening of specifically MRSA carriers
the primary niche for colonization. Watanakunakorn et al.28 among HCWs sheds light on the effectiveness of the hospital infec-
also had a similar finding of the highest recolonization after tion control measures as well as providing a basis to improve the
3 months (12 weeks) of decolonization, as in this study. flaws in the prevalent methods, if any. Although there were no
Similarity in the rate of recolonization among MRSA and MSSA MupRSA carriers in this study, the ongoing trend of an increase
carriers suggest that MRSA or MSSA carriage has no significant in mupirocin resistance emphasizes the need for prudent use of
impact on recolonization. As all the recolonized HCWs were mupirocin. As recolonization seems inevitable in some individuals,
MSSA carriers, it might be possible that MSSA has advantage the strict practice of handwashing as per the WHO guideline and
over MRSA when competing for the same niche. Although resist- refraining from the habit of nose-picking might be beneficial steps
ance to mupirocin has been implicated as one of the risk factors to prevent recolonization as well as spread of the bacteria by the
for recolonization, none of the carriers as well as recolonized car- carrier. As carriers in this study were identified only phenotypically,
riers harboured MupRSA in this study. A similar finding has been further genotyping could have helped to assess the genetic
reported by Buehlmann et al.6 as no MupRSA carriers among re- relatedness among the isolates, including transmission events.
colonized MRSA carriers.
Females were recolonized more than males, adding support to
the finding of more carriers among females in this study. All the
recolonized carriers either had the habit of nose-picking or did not
follow the WHO guideline of handwashing or both. Both recolo-
Acknowledgements
nized carriers from the Paediatrics department (including PICU We thank the participants and the entire Department of Microbiology,
Nepal Medical College.
and NICU), i.e. the department with highest recolonized carriers,
had the habit of nose-picking and did not follow the WHO guide-
line of handwashing. Overall, doctors were recolonized the most
as well as in three individual departments. Nurses had highest re-
colonization in two departments. This finding could be explained Funding
by closer contact of doctors and nurses with the patients. This study was thesis research for the partial fulfilment of the degree of
This study has shed light on the prevalence of not only Doctor of Medicine in Microbiology and the required funds were met by
S. aureus carriers (including MRSA and MupRSA) among HCWs the departmental resources.

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