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Original Article
ARTICLE IN PRESS
doi:
10.25259/IJMR_1224_2024

Methicillin-resistant Staphylococcus aureus (MRSA) carriage among the critical care personnel in a tertiary care hospital in Sikkim: An observational study

Department of Microbiology, Sikkim Manipal Institute of Medical Sciences, Sikkim Manipal University, Gangtok, India

For correspondence: Prof. Dechen Chomu Tsering, Department of Microbiology, Sikkim Manipal Institute of Medical Sciences, Sikkim Manipal University, Gangtok 737 102, Sikkim, India e-mail: drdechen@gmail.com

Licence
This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.

Abstract

Background & objectives

Persistent nasal colonisation of methicillin-resistant Staphylococcus aureus (MRSA) among healthcare personnel (HCP) remains a significant challenge. MRSA carriers are crucial to the spread of the infection, with healthcare professionals often acting as vectors for both hospital- and community-acquired MRSA. This study aimed to evaluate the MRSA carriage rate among healthcare professionals from critical care units at a tertiary care hospital in Gangtok, Sikkim. Furthermore, the study undertook to analyse antibiotic susceptibility patterns of isolated MSSA and MRSA strains, and identify associated risk factors for MRSA infection.

Methods

Three hundred samples from healthcare workers (HCW) posted in the critical care units of a tertiary care hospital were cultured and identified by routine biochemical methods. Antibiotic susceptibility test was performed by Kirby Bauer disk diffusion method for all MRSA and MSSA isolates. Association with various risk factors was understood by the Chi square test.

Results

Nineteen of the 300 participants were identified as nasal MRSA carriers having an overall carriage rate of 6.33 per cent in this study. The prevalence of MRSA was seen to be the highest among the attendants (9.52%), and the highest carriers were from the surgical Intensive Care Unit (ICUs). All the MRSA and MSSA isolates showed 100 per cent resistance to penicillin and 100 per cent susceptibility to linezolid. A significant correlation among hand hygiene practices and patient contact was reported from this study.

Interpretation & conclusions

Despite existing infection control policies, the MRSA carriage seen in HCWs in critical care units was 6.33 per cent, highlighting the need for regular systematic screening and decolonisation of all healthcare professionals to decrease the carrier status and prevent the spread of infection.

Keywords

Carriers
critical care units
healthcare workers
hospital infection control
methicillin resistant Staphylococcus aureus

Staphylococcus aureus, a prevalent bacterial pathogen, is known for its ability to induce a diverse array of infections and acquire resistance to antimicrobial agents. It is notably adept at spreading through cross transmission between patients in healthcare facilities and other institutional settings1.

Methicillin-resistant S. aureus (MRSA) isolates exhibit resistance to all penicillin and β-lactam antibiotics and were initially documented in 1961, a year after the introduction of semisynthetic penicillin, leading to its dissemination in both hospital settings and community environments2. Currently it is a high group priority pathogen linked to the emergence of antibiotic resistance3. It is an important agent of healthcare-associated infections. A systemic review and meta-analysis done from 2000 to 2021 in South Asia reported a pooled prevalence to be 9.23 per cent among HCWs (range 0.69%- 36.06%)4. Another systemic review and meta-analysis conducted from 2008 to 2017 reported the MRSA nasal colonisation rate among Indian healthcare workers (HCW) to be 11 per cent4,5.

Widespread prevalence of MRSA in healthcare settings and the increasing transmission from HCWs to patients are well-documented. Previous studies have highlighted a significant rise in nosocomial MRSA transmission6,7. MRSA infections are linked to higher morbidity, mortality, longer hospital stays, and increased healthcare costs compared to methicillin-susceptible S. aureus (MSSA) infections8. Public health agencies have issued global directives to reduce nosocomial MRSA transmission. Despite these measures, persistent nasal colonisation of healthcare personnel (HCP) by MRSA remains a significant challenge9. Carriers significantly contribute to its spread, with healthcare professionals acting as vectors for both hospital- and community-acquired MRSA10. The World Health Organisation (WHO), Centers for Disease Control and Prevention (CDC), and Indian Council for Medical Research (ICMR) have standard guidelines for infection control practices with strategies to prevent MRSA transmission and infection11-13.

With this context in mind, this study aimed to assess the MRSA carriage rate among healthcare professionals assigned to critical care units at a tertiary care hospital in Gangtok, Sikkim, to analyse the pattern of antibiotic susceptibility of the isolated S. aureus and MRSA strains and ascertain the risk factor associated with MRSA infection.

Materials & Methods

This is a hospital based observational study conducted among all the healthcare workers posted in various critical care units [medicine Intensive Care Unit (ICU), surgical ICU, neonatal and paediatric ICU, cardiac care units, neurosurgical ICU, and post operative wards, Intensive trauma unit] of a Central Referral Hospital, Gangtok, Sikkim from July 2022 – June 2023. Approval was taken from the Institutional Ethics Committee prior to the start of the study. A written informed consent was taken from the participants.

All eligible candidates were provided with a questionnaire (which was developed in-house and validated) for the assessment of various risk factors like proper hand hygiene, history of close contact with any patient, history of hospitalisation or any chronic illness, etc.

Sample collection and processing

Sterile premoistened nasal swabs were collected from the anterior nares using a standard rotating technique and sent to the laboratory for analysis. Swabs were then inoculated in blood agar and mannitol salt agar. After overnight incubation, S. aureus was identified using standard procedures by studying colony morphology, Gram staining and routine biochemical tests14.

Screening for MRSA

All isolated S. Aureus strains were screened for methicillin resistance by the Kirby-Bauer disc diffusion method by using cefoxitin discs (30 µg) on Mueller-Hinton agar (MHA).The colony was considered methicillin-resistant if the zone of inhibition was ≤21 mm as per the CLSI guideline15.

Antibiotic Susceptibility Test

Antimicrobial susceptibility test for MSSA and MRSA isolates was done by Kirby Bauer’s disc diffusion in Mueller Hinton agar against erythromycin (15 µg), penicillin (10 units), ciprofloxacin (5 µg), linezolid (30 µg), tetracycline (30 µg), clindamycin (2 µg), trimethoprim-sulfamethoxazole (23.75/1.25 µg), rifampicin (5 µg) and gentamicin (10 µg) as per the CLSI guideline15.

Statistical analysis

IBM SPSS system version 27.0 was used for statistical testing. A Chi-square test was conducted to analyse the association between categorical variables. A P value < 0.05 was considered significant for all tests.

Results

Out of the 300 participants, 70 (23.22%) were males, and 230 (76.66%) were females. Maximum participants, 202 (67.33%), belonged to the age group of 25-35 yr, the rest were (18.33%) between 36 and 45 yr. The age of the participants ranged from 23-58 yr (mean=31.94, SD=7.222). Among the participants, 44.66 per cent were staff nurses, 27 per cent were doctors, 13 per cent were attendants, seven per cent were housekeeping staff, and 6.33 per cent were physiotherapists and OT technicians. Most participants (51.6%) had 1-5 yr experience in critical care, 21.33 per cent had 6-10 yr, 11.66 per cent had 11-20 yr, and 1.33 per cent had 21-40 yr. Educationally, 27 per cent were graduates, 23.33 per cent were postgraduates, and 3.33 per cent had only primary education (Table I).

Table I. Demographic profile of the participants
Parameters Number Percent (%)
Age (yr)
<25 21 7
25–35 202 67.33
36–45 55 18.33
46–55 21 7
>56 1 0.33
Sex
Male 70 23.33
Female 230 76.67
Profession
Doctors 81 27
Staff nurses 140 46.66
Attendants 39 13
Housekeeping staff 21 7
Others 19 6.33
Work experience (yr)
<1 42 14
1-5 155 51.6
6–10 64 21.33
11–20 35 11.66
21–40 5 1.33
Educational qualification
Primary school 10 3.33
Secondary school 34 11.33
High secondary school 15 5
Graduate 171 27
Post graduate 70 23.33

The most predominant organism isolated was coagulase-negative Staphylococci, 194 (64.7%). A total of 79 (26.3%) S. aureus colonies were isolated, among which 19 (24.05%) were methicillin-resistant. Nineteen (6.3%) nasal swabs processed showed no growth, and 4 (1.3%) swabs each showed growth of other organisms (namely gram-negative bacilli, micrococci, and candida species).

Of all the HCWs screened from critical care units, 19 were identified as MRSA carriers with nasal colonisation, while 281 were non-carriers. This study found a 6.33 per cent prevalence of MRSA nasal carriage in HCWs working in critical units.

Among the 230 female participants screened, 5.65 per cent were MRSA nasal carriers, compared with 10 per cent in the 70 male participants. Educationally, 26.67 per cent of MRSA carriers had completed Higher Secondary School, 6.44 per cent were graduates, 5.89 per cent had secondary education, and 5.72 per cent were postgraduates. The highest MRSA prevalence of 9.52 per cent was among attendants, followed by 7.69 per cent of housekeeping staff, 6.17 per cent doctors, and 6.42 per cent staff nurses. No MRSA carriers were reported among physiotherapists and OT technicians (Table II).

Table II. Demographic analysis of the participants
Parameters Non carriers (%) MRSA carriers (%) Total (%) P value
Age (yr)
< 25 19 (90.47) 2 (9.53) 21 (7) 0.599
25–35 188 (92.61) 15 (7.38) 203 (67.66)
36–45 54 (98.18) 1 (1.82) 55 (18.33)
46–55 19 (95) 1 (5) 20 (6.66)
>56 1 (100) 0 1 (0.33)
Sex
Male 64 (91.42) 6 (8.57) 70 (23.33) 0.38
Female 217 (94.34) 13 (5.65) 230 (76.67)
Profession
Doctors 76 (93.82) 5 (6.17) 81 (27) 0.881
Staff nurse 131 (93.57) 9 (6.42) 140 (46.66)
Housekeeping 36 (92.30) 3 (7.69) 39 (13)
Staff
Attendants 19 (90.47) 2 (9.52) 21 (7)
Others 19 (100) 0 19 (6.33)
Work experience (yr)
<1 39 (92) 3 (7.14) 42 (14)
1-5 145 (93.54) 10 (6.45) 155 (51.6) 0.189
6–10 60 (93.75) 4 (6.25) 64 (21.33)
11–20 33 (94.28) 2 (5.71) 35 (11.66)
21–40 5 (1000) 0 5 (1.33)
Education
Primary school 10 (100) 0 10 (3.33)
Secondary school 32 (94.11) 2 (5.89) 34 (11.33) 0.041*
H S school 11 (73.33) 4 (26.67) 15 (5)
Graduate 160 (93.56) 11 (6.44) 171 (57)
Post Graduate 66 (94.28) 4 (5.72) 70 (23.33)

P*<0.05 significant association

MRSA carriers were distributed across various critical care units: 16.66 per cent in the neurosurgical ICU, 12.12 per cent in the orthopaedic ITU, 10.86 per cent in the surgical ICU, 6.81 per cent in the post-operative OT, and 2.56 per cent in the medicine ICU. No MRSA carriers were reported from the paediatric ICU, neonatal ICU, post-operative OBG unit, or cardiac care units (Table III).

Table III. Distribution of MRSA carriers in different critical care units
Location Non-carriers (%) MRSA carriers (%) Total (%)
Medicine ICU 38 (97.43) 1 (2.56) 39 (13)
Surgical ICU 41 (89.13) 5 (10.86) 46 (15.33)
Neurosurgical ICU 30 (83.33) 6 (16.66) 36 (12)
Orthopedic ITU 29 (87.87) 4 (12.12) 33 (11)
Paediatric ICU 24 (100) 0 24 (8)
Neonatal ICU 22 (100) 0 22 (7.33)
Post operation observation (OT) 41 (93.18) 3 (6.81) 44 (14.66)
Post Operation OBG 36 (100) 0 36 (12)
Cardiac care unit 20 (100) 0 20 (6.66)
Total 281 (93.66) 19 (6.33) 300 (100)

ICU, intensive care unit; OT, operation theatre; OBG, obstetrics and gynecology; ITU, intensive trauma unit

Antibiotic susceptibility test

All the MSSA isolates were 90 per cent sensitive to gentamicin, 85 per cent to tetracycline, and 60 per cent to trimethoprim/sulfamethoxazole. MSSA isolates showed 40 per cent sensitivity to erythromycin and 14 per cent sensitivity to ciprofloxacin. All the MSSA isolates showed 100 per cent susceptibility to linezolid and rifampicin. All the MSSA isolates were resistant to penicillin (Fig. 1).

Antibiotic susceptibility pattern of MSSA.
Fig. 1.
Antibiotic susceptibility pattern of MSSA.

All the isolates of MRSA showed 100 per cent sensitivity to linezolid, 94.73 per cent to rifampicin, 84.21 per cent to tetracycline, 78.94 per cent to trimethoprim sulfamethoxazole and 73.68 per cent to gentamicin. While MRSA isolates were 47.36 per cent sensitive to clindamycin, 42.1 per cent sensitive to erythromycin and 10.52 per cent to ciprofloxacin (Fig. 2).

Antibiotic susceptibility pattern of MRSA isolates.
Fig. 2.
Antibiotic susceptibility pattern of MRSA isolates.

MRSA carriage rate and its association with various risk factors

Among MRSA carriers, 92.85 per cent rarely followed hand hygiene practices, 7.4 per cent followed them occasionally, and only 0.86 per cent adhered to them regularly. This observation was made following a regular hand hygiene audit done by the hospital infection control team of the hospital. The association between hand hygiene practices and MRSA carriage was found to be clinically significant (P<0.05).

Among the 200 participants with recent history of close contact with a patient within last four weeks, nine per cent (n=18) were MRSA positive, and one per cent (n=1) MRSA carriers had no history of close contact with any patient. Among 72 participants with a recent history of close contact with MRSA patients within the last four wk, 22.23 per cent (n=16) were MRSA carriers. Seven per cent of the participants were diabetic, 5.66 per cent had a history of chronic respiratory illness, 25.66 per cent had used antibiotics in the last six months, and 3.66 per cent had been hospitalised in the previous year.

This study revealed significant associations between MRSA carriage and hand hygiene practices, as well as close contact with patients. Among MRSA carriers, 92.85 per cent reported rarely following hand hygiene protocols, while only 0.86 per cent consistently adhered to them, showing a significant correlation between hand hygiene and MRSA carriage (P<0.05). Furthermore, nine per cent of participants with recent close patient contact were MRSA positive, indicating a significant link between patient contact and MRSA carriage (P<0.05). Additionally, 22.23 per cent of those with close contact with MRSA patients in the past four wk were carriers, reinforcing this association (P<0.05). No significant associations were found between MRSA carriage and diabetes, chronic respiratory illness, recent antibiotic use, or hospitalisation within the past year. These findings highlight the importance of hand hygiene, and the risks associated with close patient interactions with respect to controlling MRSA spread (Table IV).

Table IV: MRSA carriage rate and its association with various risk factors
Parameters Non carriers (%) MRSA carriers (%) Total (%) P value
Hand hygiene
Always 230 (99.13) 2 (0.86) 232 (77.33) 0.000*
Occasionally 50 (92.59) 4 (7.40) 54 (18) χ2 = 188.49 df = 2
Rarely 1 (7.14) 13 (92.85) 14 (4.66)
Close contact with patients in the last 4 wk
Yes 182 (91) 18 (9) 200 (66.66) 0.007*
No 99 (99) 1 (1) 100 (33.33) χ2 = 7.192 df = 1
Close contact with MRSA patients
Yes 56 (77.77) 16 (22.23) 72 (24) 0.000*
No 225 (98.68) 3 (1.31) 228 (76) χ2 = 40.31 df = 1
Known case of diabetes mellitus
Yes 19 (90.47) 2 (9.52) 21 (7) 0.534
No 262 (93.90) 17 (6.09) 279 (93)
Known case of chronic respiratory illness
Yes 15 (88.23) 2 (11.76) 17 (5.66) 0.344
No 266 (93.99) 17 (6.01) 283 (94.34)
Use of antibiotics in the last 6 months
Yes 70 (90.90) 7 (9.01) 77 (25.66) 0.249
No 211 (94.61) 12 (5.38) 223 (74.34)
Inpatient hospital treatment in the last 12 months
Yes 10 (90.90) 1 (9.10) 11 (3.66) 0.702
No 271 (93.77) 18 (6.22) 289 (96.34)

P*<0.05 significant association

Discussion

It is essential to identify the carriers of MRSA among HCWs within hospital settings, specifically those employed in critical care units, as they serve as potential conduits for the spread of nosocomial illnesses, which prolong hospital stays.

In this study, 300 nasal swabs from HCWs in critical care units identified a 6.33 per cent MRSA carriage rate, which was comparable to previous studies conducted by Goyal et al16 in Delhi (6.6%), a study from Mysore (6.5%)17, Latha et al18 in Manipal (6.4%), and Singh et al19 in Bhubaneswar (7.5%)16-19. Contrary to our findings, other studies have reported varying MRSA colonisation rates among HCWs. Another study from Mangalore, Karnataka20 documented a 2.5 per cent prevalence in Mangalore, while Sridharan et al21 reported an 11.5 per cent carriage rate in Meerut.

A global study by Albrich and Harbarth, involving a literature review of 33,318 HCWs screened from January 1980 to March 2006, found a 4.6 per cent MRSA infection or colonisation rate10. Additionally, a systematic review and meta-analysis by Latha et al5 reported a pooled MRSA nasal carriage prevalence of 11 per cent among Indian HCWs.

This disparity can be attributed to differences in study design, including variations in sample size, methodologies, and detection techniques. Additionally, geographical regions and institutions may exhibit different MRSA prevalence rates.

In our study, 8.57 per cent (6) of the total MRSA carriers were males, and 5.65 per cent (13) were females. Similar results were seen in a study conducted by Singh et al19 where the carriage rate of MRSA among males was 9.1 per cent and 6.5 per cent among females. Giri et al22 from Nepal also reported a higher prevalence among males (8.7%) than females.

In this study, MRSA prevalence was highest among attendants (9.52%), followed by housekeeping staff (7.69%), staff nurses (6.42%), and doctors (6.17%). This contrasts with a study17 in Mysore, where the highest prevalence was among doctors (28.4%) and nursing interns (21.1%)17. Other Indian studies like the one by Singh et al19 have also reported a higher MRSA carriage prevalence among the staff nurses (22.1%), which is in contrast to this study.

The mechanism underlying MRSA nasal carriage is complex and not fully understood. The increased rate among nurses presents a notable epidemiological concern, as their frequent patient interactions make them potential reservoirs for infection, thereby perpetuating MRSA within the hospital setting.

This study reports the highest MRSA nasal carriage prevalence among HCWs in the neurosurgical ICU (16.66%), followed by the orthopedics ITU (12.12%), surgical ICU (10.86%), post-operative OT (6.81%), and medicine ICU (2.56%). Similarly, Khanal et al23 found a high frequency of MRSA carriers in the surgical ICU and post-operative ward (28.6%). This may be due to high workload, overcrowding, and frequent wound care in these units, increasing MRSA transmission23.

MRSA is associated with adverse clinical outcomes in ICUs and poses a significant challenge to hospital infection control. ICUs play a critical role in the widespread dissemination of MRSA, as individuals frequently move between various healthcare settings, including hospital wards and other medical facilities19. A significant association between MRSA carriage and educational qualification was seen in this study (P=0.041). This aligns with the study by Maroof et al24 from Srinagar, which also found a higher prevalence among graduates.

The main obstacle to effective infection control protocols is rigorous adherence. Regular education and skill development for new HCWs, with active participation, can be a straightforward and efficient strategy to prevent the transmission of antibiotic-resistant bacteria like MRSA.

In this study, S. aureus isolates exhibited 100 per cent resistance to penicillin, consistent with findings by Bala et al25 and Goyal et al16, though Kausalya et al26. and Rahman et al27 reported 71.5 per cent and 75 per cent resistance, respectively. Resistance to ciprofloxacin was 86 per cent, aligning with Ramakrishnan et al20 and Singh et al19 (80 per cent), while Rahman et al27 and Agarwal et al28 reported lower resistance rates of 47.5 per cent and 50 per cent, respectively27,28. Resistance rates in our study were 60 per cent for erythromycin, 58 per cent for clindamycin, and 40 per cent for trimethoprim/sulfamethoxazole, similar to Singh et al19 (58% for erythromycin) and Ramakrishnan et al20 (60%). Lower clindamycin resistance was reported in Singh et al19 (20%) and Rahman et al27 (15.91%) as compared to the present study. Gentamicin and tetracycline susceptibility were 90 per cent and 85 per cent, respectively, similar to Aila et al29 (96.8% and 85.8%) and Giri et al22 (100% and 90.9%). Linezolid and rifampicin susceptibility was 100 per cent, consistent with Bala et al25, and Giri et al22.

Among MRSA isolates, 100 per cent resistance to penicillin was observed, consistent with Bala et al25 and Goyal et al16. Resistance rates were 89.47 per cent for ciprofloxacin, 57.89 per cent for erythromycin, and 52.63 per cent for trimethoprim/sulfamethoxazole. MRSA strains showed 100 per cent susceptibility to linezolid and high sensitivity to rifampicin (94.73%), tetracycline (84.21%), trimethoprim/sulfamethoxazole (78.94%), and Gentamicin (73.68%). This aligns with Aila et al29, who reported 88.2 per cent sensitivity to rifampicin, 86.3 per cent to tetracycline, and 92.2 per cent to gentamicin. In contrast, Khanal et al23 reported higher resistance to gentamicin (42.9%) and lower resistance to ciprofloxacin (14.3%) and trimethoprim/sulfamethoxazole (28.6%)23. Clindamycin resistance in the present study was 52.63 per cent, similar to Singh et al19 (50%) and Maroof et al24 (62.5%), but contrasting with Giri et al22, who reported high sensitivity (83.3%).

The variability in resistance rates among different antimicrobial agents reflects factors such as regional prescribing practices, patient demographics, and microbial characteristics. Antibiotic resistance in hospitals is primarily driven by the overuse, misuse, and inappropriate prescription of antibiotics for both community-acquired and hospital-acquired infections. Routine in vitro susceptibility testing for clindamycin is not reliable for identifying inducible resistance mediated by the erm gene, leading to treatment failure. This can be avoided by implementing a simple D-test for routine diagnostic procedure for accurate detection of inducible clindamycin resistance30. The absence of strict regulations on antibiotic prescriptions, coupled with the accessibility of over-the-counter antibiotics, further aggravates this problem. Consequently, treating S. aureus infections in hospitals with these antibiotics may be ineffective due to high resistance rates.

Our study identified significant risk factors for MRSA colonisation, including non-adherence to hand hygiene practices (P<0.05), recent close interactions with patients (P=0.007), and proximity to MRSA carriers (P<0.05). However, antibiotic use, hospitalisation, and chronic medical conditions did not show a statistically significant association with MRSA carriage. The Healthcare Infection Control Practices Advisory Committee emphasises that the absence of an outbreak does not eliminate transmission risk31. Therefore, healthcare institutions should implement regular screening protocols for healthcare personnel, both during recruitment and periodically thereafter.

Some limitations of this study only include that it focussed on the HCPs posted in critical care units. Also, follow up of the identified carriers was not done. Inducible clindamycin resistance test (D test) was not done for the isolates as this study was for screening of nasal carriers and not patients. Furthermore, the absence of comparison with genotypic methods to ascertain the presence of resistance genes represents another notable limitation due to constraints pertaining to time, funding, and the availability of laboratory infrastructure.

Overall, this study found an MRSA nasal carriage rate of 6.33 per cent among HCWs in critical care units, with the highest prevalence among attendants and housekeeping staff. This highlights the need for targeted education and training to enhance infection control practices in these groups. Asymptomatic MRSA carriers among HCPs are of significance due to their potential to transmit the pathogen, increasing patient morbidity, mortality, and healthcare costs. Therefore, strict enforcement of infection control measures is crucial to reduce MRSA carriage and transmission in hospital settings.

Financial support & sponsorship

None.

Conflicts of Interest

None.

Use of Artificial Intelligence (AI)-Assisted Technology for manuscript preparation

The authors confirm that there was no use of AI-assisted technology for assisting in the writing of the manuscript and no images were manipulated using AI.

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