Prevalence and determinants of methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus carrier among staff of a tertiary eye hospital in Saudi Arabia.

OBJECTIVES: The objective of this study was to estimate the prevalence and risk factors of methicillin-sensitive Staphylococcus aureus (MSSA) and methicillin-resistant S. aureus (MRSA) carriers among staff of a tertiary eye hospital in Saudi Arabia.
METHODS: This retrospective study was conducted in 2019. Nasal and axillary swabs of health-care staff were used to determine carriers of MRSA. Bacteria were identified by culture and sensitivity tests. These isolates were grouped as antibiotic resistant, sensitive, and others not in the S. aureus group. Demographics and other determinants were associated with carrier status.
RESULTS: We evaluated the carrier status of 430 staff. There were 110 (24.9%; 95% confidence interval [CI]: 21.5, 29.7) S. aureus-positive staff, 21 (11.7%; 95% CI: 11.7, 26.4) of who carried the MRSA strain. Carrier status was significantly higher among physicians (31%) compared to nurses (22.5%) and other staff (5.7%) (P < 0.001). MRSA carrier status was significantly associated with >5 years of employment at the eye hospital (P = 0.02). MRSA was significantly associated with staff who were of Indian nationality (75%) compared to other nationalities (P = 0.04) and those who were at the hospital for <5-year stay compared more than 5 years at the hospital (P = 0.001). All carriers responded to decolonization treatment.
CONCLUSIONS: The high prevalence of MRSA and relatively easy treat MRSA carriers points at the need for universal screening for MRSA carriers among eye health staff. Copyright:

Introduction

Staphylococcus aureus is one of the most common microbes that cause ocular infections such as conjunctivitis, keratitis, and endophthalmitis.[1] Approximately 35% of general population and 50%–66% of health-care workers (HCWs) become colonized with this organism.[23] Methicillin-resistant S. aureus (MRSA) and methicillin-sensitive S. aureus (MSSA) cause serious ocular infections in different age groups. Furthermore, MRSA is associated with multidrug-resistant ocular wound infections in the postoperative period.[4]

MRSA infections may be acquired from an endogenous source in colonized patients, or infection may occur in health-care settings. In many cases, asymptomatic HCWs act as carriers of MRSA causing hospital-acquired infections in patients.[5] MRSA/MSSA colonization in patients transferred from other hospitals can also be a source of transmission to HCWs and to other patients.[6] Decolonization of MRSA/MSSA in HCW has been recommended to reduce the prevalence of carriers and transmission.[7] The outcomes of tests to determine whether an individual is an MRSA/MSSA carrier also depend on the anatomic site selected for sample collection.

MRSA colonization is known to involve the anterior nares, axilla, and groin with the highest yield from nasal specimens.[8] While benefits of routine MRSA surveillance in HCW are unclear and controversial, some institutions perform targeted screening of asymptomatic employees routinely, while others perform screening only during MRSA outbreaks to identify carriers and prevent transmission from HCW to patients.[9]

There is a relative paucity of information on the carrier status of MRSA/MSSA in HCWs at eye hospitals, especially in the Kingdom of Saudi Arabia. In this study, we investigated the extent of MRSA and MSSA colonization among eye HCWs at King Khaled Eye Specialist Hospital (KKESH) during 2018–2019. KKESH is a tertiary care eye hospital with unique patient population in the Gulf region and strives to achieve best practices in patient care. With the aim of reducing hospital-acquired MRSA infection, a pilot study was performed to observe the benefits of routine screening of HCW for MRSA. In this study, we investigated the MRSA/MSSA carrier status by testing different anatomic locations and the subsequent outcomes following decolonization of S. aureus.

Methods

A retrospective review was performed of health records at KKESH, Riyadh, Saudi Arabia. As per policy, the Institutional Research and Ethical Committee reviewed and approved this project (2004-P). This study adhered to the tenets of the Declaration of Helsinki. KKESH staff were recruited for this study and provided samples between December 2018 and November 2019. The study was done using data from the existing HCW screening program of the institution. A pretested data collection form was used for data collection. It had two components; clinical and demographic information was collected from the hospital information system by reviewing employee health records. Data were collected on the presence/absence of common disorders such as diabetes, hypertension, asthma, allergic manifestations, and the immunocompromised status. Data were collected on the testing performed at the more recent follow-up appointment at the employee clinic. Records were collected if they were under treatment at the institute or from their health chart at the most recent employment contract renewal.

Laboratory tests were performed to assess if an individual was a S. aureus carrier using conventional bacterial cultures and sensitivity of the isolates to methicillin.

Nasal swabs and axillary swabs were obtained for bacterial cultures. Swabs were inoculated onto sheep blood agar (SBA), chocolate agar plate (CAP), and mannitol salt agar (MSA).

Both SBA and CAP were incubated in an atmosphere of 5%–10% CO2 at 37°C for 2 days. MSA was incubated at 35°C for 18–24 h in ambient air. After 18–24 h, the plates were examined for isolated colonies of Staphylococcal species. A Gram stain and biochemical tests including catalase and coagulase tests were performed for presumptive identification of S. aureus. Final identification of isolates was confirmed in VITEK®2 instrument, with the cefoxitin disc and CHROMagar MRSA for confirmation of identification and susceptibility.

Isolates with a cefoxitin disc zone diameter of ≤21 mm as per the Clinical and Laboratory Standards Institute criteria and growth in CHROMagar MRSA of rose to mauve colonies were considered to be MRSA.[10]

The decolonization treatment protocol in this study was similar to the USA Centers for Disease Control (CDC) guidelines and included mupirocin 2% three times a day for 5 days applied inside the nostrils and chlorhexidine 4% once daily for 5 days applied on axillary hair and skin.[11]

Data were entered into an Access® spreadsheet (Microsoft Corp., Redmond, WA, USA). Data were analyzed using the Statistical Package for the Social Sciences. (SPSS 25) (IBM, Armonk, NY, USA). The prevalence rate of MRSA and MRSR, their 95% confidence interval (CI) were estimated. A possible projected number of MRSA and MRSS were calculated among KKESH staff.

The outcome variable; participant's MRSA status (present or absent) was correlated to the continuous variables such as age by using bivariate correlation and Pearson coefficient. A two sided P-value was also estimated. The outcome was associated with the gender by using Student's t-test to calculate odds ratio (OR), its 95% CI, and two-sided P value. To associate the MRSA carrier status to the country of residence of the staff health, we used Chi-square value, degree of freedom, and two-sided P value. P <0.05 was considered as statistically significant. The conversion rate of laboratory-confirmed MRSA to a noncarrier following treatment was also determined.

Results

The study sample was comprised of 430 hospital staff who were tested over 2 years at our institution. Table 1 presents the demographic profile-associated health disorders of the participants. Over 75% of participants were females. Nearly 33% were local Saudi citizens while about 66% were recruited from other countries as expat employees. Nearly 66% of the participants were nursing staff who were screened over the duration of this study.

Table 1

Demographic profile of participating health staff from a tertiary eye hospital in Saudi Arabia

	n (%)
Gender
Male	117 (27.2)
Female	313 (82.8)
Working in hospital (years)
5 or less	168 (39.1)
>5	262 (60.9)
Type of work
Doctor	42 (9.8)
Nurse	284 (66.0)
Optometrist	4 (0.9)
Outpatient technicians	32 (7.4)
Laboratory technicians	24 (5.6)
Interpreters	13 (3.0)
Other	31 (7.2)
Nationality
Saudi	140 (32.6)
Philippines	150 (34.9)
Indian	70 (16.3)
Malaysian	35 (8.1)
Other	35 (8.1)
Systemic ailments
Diabetes	16 (3.7)
Genetic ailments	0
Asthma	18 (4.2)
Thalassemia	0
Age (years), mean±SD	38.6±10.3

SD: Standard deviation

There were 110 (24.9%, 95% CI: 21.5, 29.7) participants who had a positive culture for S. aureus. Among these participants, 21 (11.7%, 95% CI: 11.7, 26.4) were positive for MRSA while the remaining 88.3% were MSSA. Table 2 presents the results from swabbing. Nasal swabs resulted in a higher number of positive cultures for S. aureus compared to the axillary specimen; MSSA was more common in nasal specimens than in axillary swabs.

Table 2

Staphylococcus aureus carrier and methicillin resistance status of health staff at a tertiary eye hospital in Saudi Arabia

	Examined	n (%)	95% CI
Nasal or axillary swab
S. aureus
Positive	430	110 (24.9)	21.5-29.7
Negative		320 (75.1)
Methicillin response
Sensitive	110	89 (88.3)	11.7-26.4
Resistant		21 (11.7)
Nasal swab
S. aureus
Positive	430	106 (24.7)	20.6-28.7
Negative		324 (75.3)
Methicillin response
Sensitive	106	86	10.6-25.2
Resistant		19 (17.9)
Axillary swab
S. aureus
Positive	430	8 (1.9)	0.6-3.1
Negative		422 (98.1)
Methicillin response
Sensitive	8	6	0.0-55.0
Resistant		2 (20)

CI: Confidence interval, S. aureus: Staphylococcus aureus

All 21 MRSA-positive staff underwent decolonization treatment, and they subsequently were negative as determined by bacterial culture after 1 month.

Table 3 presents the association between the carrier status and MRSA status to different determinants. The S. aureus carrier status was statistically significantly higher among physicians (31%) as compared to nurses (22.5%) and other staff (5.7%) (P < 0.001). The carrier status was statistically significantly associated with more than 5 years of continuous employment at KKESH compared to <5 years of employment (P = 0.02). Gender, nationality, and other comorbidities were not significantly associated with carrier status.

Table 3

Determinants of Staphylococcus aureus-positive cases and methicillin-resistant Staphylococcus aureus cases among health staff from a tertiary eye hospital in Saudi Arabia

Determinant	Total, n (%)	Staphylococcus aureus			Response to methicillin
		Positive	Negative	Validity	Sensitive	Resistant	Validity
Gender
Male	117 (27.2)	38	79	OR=1.3 (0.8-2.1), P=0.25	7	31	OR=0.9 (0.3-2.6), P=0.9
Female	313 (82.8)	72	241		14	58
Work type
Doctor	42 (9.8)	13	29	χ2=17, Df=2, P<0.001	3	10	χ2=5, Df=2, P=0.02
Nurses	284 (66.0)	64	220		12	52
Other	104 (24.2)	6	98		6	0
Years in KKESH
≤5	168 (39.1)	33	135	OR=0.6 (0.2-0.9), P=0.02	7	27	OR=19.7 (2.3-167), P=0.001
>5	262 (60.9)	77	185		1	76
Nationality
Saudi	140 (32.6)	42	98	χ2=1, Df=4, P=0.8	10	32	χ2=4, Df=4, P=0.04
Philippines	150 (34.9)	33	117		7	26
Indian	70 (16.3)	7	63		3	4
Malaysian	35 (8.1)	19	16		1	18
Other	35 (8.1)	9	26		0	9
Health ailment
Present	34	12	21	OR=1.2 (0.6-2.5), P=0.6	1	11	OR=0.3 (0.05-2.9), P=0.3
Absent	396	98	299		20	78

P<0.05 is statistically significant. OR: Odd ratio, χ2: Chi-square test, Df: Degrees of freedom, KKESH: King Khaled Eye Specialist Hospital

MRSA carrier status was statistically significantly associated with staff of Indian nationality (75%) compared to other nationalities (P = 0.04) and those who were employed for <5-year stay at KKESH at the time of testing (P = 0.001). Gender, type of work, and other comorbidities were not significantly associated with MRSA carrier status.

Discussion

In the present study, we report that one in four health staff at a tertiary eye hospital in Central Saudi Arabia were carriers of S. aureus and nearly one in five of these individuals carried the methicillin-resistant strain. All MRSA carriers responded to the treatment and were cleared of MRSA within a month. Physicians as the group were the most common S. aureus carriers compared to other health staff. Staff with a longer tenure at our hospital at the time of testing had higher rates of S. aureus-positive status. Interestingly, Indian nurses and those employed for <5 years had significantly higher MRSA-positive carrier status. Nasal swabbing reliably detected the carrier status while the axillary swab was not consistent in detecting carrier status.

A previous study reported that the incidence of ocular infection due to S. aureus was 12.9% and 13% of these cases were MRSA.[12] The risk of keratitis and conjunctivitis due to MRSA has increased.[13] In MRSA-induced ocular infections, the vision can be compromised despite treatment. Hence, efforts at prevention are recommended. Households with individuals who work at health-care facilities (OR = 9) and those who regularly visit health-care facilities (OR = 24) have a higher prevalence of MRSA than the normal, healthy population.[14] Therefore, the S. aureus status among ophthalmic staff noted in the current study can be used to implementing strategies to mitigate the risk of MRSA infections in patients seeking eye care.

The overall rate of S. aureus in health staff in the present study was 24.9%. In a study in another university hospital in Central Saudi Arabia, the S. aureus carrier rate was 40% and an Indian study reported a rate of 43.6%.[1516] Our outcome concurs with Turkish and Iranian studies that the reported rates were 24% and 27%, respectively.[1718] Different methods of laboratory confirmation for MRSA and type of work of health staff could be explained the differences in incidence between our outcomes and previous Saudi and Indian studies.[1516] However, the high incidence noted in different studies justifies that this is a health issue that warrants periodic screening. We did not find gender variation in carrier status among ophthalmic staff. This finding contrasted with the findings of another study in Saudi Arabia where males had a higher risk of being S. aureus carriers than female health staff.[15] An Indian study reported that female nurses had a higher rate of MRSA-positive carrier status than males.[16] Thus, gender variation is difficult to explain based on the current literature.

Physicians had a statistically significantly higher carrier rate both for S. aureus and MRSA than nurses in our study. This observation concurs with Kathandki et al.'s study.[17] In contrast, an Argentinian study noted higher rates of carrier status in technicians compared to physicians. Given the mixed outcomes from our study and the current literature, the type of hospital work may not a predictor of MRSA status, but perhaps, personal hygiene could play more role in determining carrier status among health staff.

In the current study, staff with a working history of more than 5 years had a higher risk of a positive S. aureus carrier status than those with a tenure <5 years. However, the MRSA carrier status was significantly higher in staff working for <5 years. The carrier status in the current study was positively correlated to a previous Saudi study.[15] The lower risk of MRSA in staff working at our institution for a longer period could reflect change in their personal hygiene over time or less exposure to those with MRSA in the later part of their career at the eye hospital.

The variation in the S. aureus-positive rate and MRSA rate did not differ based on nationality of eye health staff in our study. However, the rate was higher in Saudi nationals compared to expatriate staff both for S. aureus and MRSA. A few Indian nurses might have resulted in a higher proportion of MRSA carriers. However, this observation should be interpreted with a caution due to the possibility of a chance observation. This issue needs further investigation with a larger sample for definitive conclusions. The health staff with a past history of working in countries with endemic MRSA were found to have a higher rate of MRSA-positive carrier status.

In our study, we collected swabs from the nasal and the axilla of each staff member enrolled in this study. The collection of sample from the axilla was marginally beneficial in determining carrier status of the health staff. However, a study from South Africa noted that colonization of extranasal sites was associated with persistent MRSA.[19] Thus, we recommend the collection of nasal samples and from the axilla if resources are adequate.

This US CDC recommends the topical application of mupirocin for decolonization of MRSA. In our study, this regiment achieved 100% decolonization. This treatment is an easy and user-friendly method compared to treatment with vancomycin that is a standard treatment for S. aureus resistance to many antibiotics.[1620]

Our study has some limitations. The risk of carrier status was higher in health staff with chronic skin diseases and poor hygiene practices.[21] We did not review these factors in our study.

Conclusions

Importance of MRSA in hospital settings is an established fact. The paper adds the same information for eye settings. The S. aureus carrier and MRSA strain are found in high prevalence among eye health-care staff. The high prevalence and the easy treatment for MRSA carriers favor universal screening for MRSA among eye care staff. Therefore, we recommend screening the entire health staff at this institute and undertake period assessments of their carrier status.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.