Risk Factors for Methicillin-Resistant Staphylococcus aureus Carriage among Patients at Admission to the Surgical Ward in a Resource-Limited Hospital in Indonesia

Abstract.

This study aimed to identify risk factors for methicillin-resistant Staphylococcus aureus (MRSA) carriage among patients at admission to the surgery ward in a resource-limited hospital in Indonesia. A case–control study was performed including 65 MRSA carriage patients and 132 non-MRSA carriage patients screened at admission to surgery wards in a hospital in Malang, East Java. For MRSA screening, swabs were obtained from nares and throat, cultured in an enrichment broth followed by subculturing onto CHROMagar^™ MRSA; suspected colonies were confirmed by polymerase chain reaction. Patients referred from other hospitals, patients transferred from the surgical acute care unit, patients that had a surgical procedure within 3 months before admission, and immunocompromised patients were more likely to be MRSA carriers at admission to the surgery wards. Selective MRSA screening of patients according to such risk factors at admission would efficiently detect MRSA carriers and may help control MRSA dissemination in surgery wards in limited-resource settings.

Health-care-associated infections caused by methicillin-resistant Staphylococcus aureus (MRSA), including bloodstream infection, pneumonia, and surgical site infection, lead to high-cost patient care, extended length of stay, high morbidity, and mortality.^1,2 Nasal carriage plays a role in the transmission of MRSA in the hospital setting.³ Our previous study revealed a high prevalence of MRSA carriage at discharge from surgery wards (8.0%).⁴ In such endemic settings, active screening of all patients for MRSA carriage at admission is recommended for infection prevention and control purposes. However, such universal screening is unlikely to be conducted in low-resource settings in developing countries including Indonesia because of the relatively high costs. Selective screening based on risk factor analysis is potentially much more efficient and, therefore, more feasible in such settings. This study aimed to analyze the risk factors for MRSA carriage among patients at admission to surgery wards of a tertiary care hospital in Indonesia.

We performed a case–control study including 65 MRSA carriage patients and 132 non-MRSA carriage patients screened at admission in the surgery ward of Dr. Saiful Anwar Hospital (tertiary care hospital; 810 beds), Malang, Indonesia, between July 2012 and August 2013. The study was approved by the medical ethics committee (no. 129/EC/KEPK-JK/05/2012). A case of MRSA carriage was defined as a patient from whom MRSA could be isolated from either anterior nares or throat. A non-MRSA carriage patient was defined as a patient from whom MRSA could not be isolated from either anterior nares or throat (this patient could harbor methicillin-susceptible S. aureus [MSSA] or other species of bacteria at these sites). Patients were enrolled prospectively. All surgery patients were eligible for inclusion. However, surgery patients already admitted more than 48 hours before the moment of enrollment were excluded. The MRSA screening was carried out by culturing of anterior nares and throat using dry cotton swabs (Deltalab, Rubi, Spain) after patients had given informed consent within 48 hours of admission. One swab was used for both anterior nares by rubbing the swab in each nostril (the “nose-picking area”). The throat was cultured with another swab by rubbing the tonsillar fossa. Swabs were directly inoculated into phenol red mannitol broth (BBL, Le Pont de Claix, France), incubated overnight at 37°C and then subcultured onto MRSA CHROMagar^™ medium (ITK Diagnostics, Uithoorn, the Netherlands) for 24–48 hours at 37°C. Typical colonies of S. aureus were confirmed with Staphaurex^®Plus (Remel, PT.Dipa Puspa Labsains, Indonesia) and subsequently identified by mass spectrometry (MALDI-TOF, Bruker, the Netherlands). Detection of mecA gene was performed by polymerase chain reaction.⁵ Data on age, gender, prior admission room, hospitalization within the past 12 months, surgical procedure within the past 3 months, immunocompromised status (patients with diabetes mellitus, chronic kidney disease, malignancy with either chemotherapy or radiotherapy, congestive heart disease; those with human immunodeficiency virus infection; and those with regular steroid usage), and open skin lesions were included in the risk factor analysis. Data were analyzed with multiple logistic regression analysis using statistical software packages SPSS, version 16.0 (Chicago, IL). A P value of < 0.05 was considered as significant.

Among the 65 MRSA carriers, we isolated MRSA from the nares only in 31 (47.7%) cases, from the throat only in 19 (29.2%) cases, and from both nares and throat in 15 (23.1%) cases. In addition, we found that 42/132 (31.8%) patients that were free from MRSA did carry MSSA strains. Factors associated with MRSA carriage among patients at admission to surgical wards in the univariate analysis were prior admission room (P < 0.001), hospitalization within the past 12 months (P = 0.007), surgical procedure within the past 3 months (P = 0.008), immunocompromised status (P = 0.084), and open skin lesions (P = 0.098). Multiple logistic regression analysis showed that patients referred from other hospitals (odds ratio [OR] 7.7, 95% confidence interval [CI₉₅] 1.2–49.1), patients transferred from the surgical acute care unit (OR 5.6, CI₉₅ 2.7–11.6), patients that had a surgical procedure within three months before admission (OR 6.7, CI₉₅ 2.3–19.4), and immunocompromised patients (OR 7.3, CI₉₅ 1.6–33.9) were more likely to be MRSA carriers at admission to the surgery wards (Table 1).

Table 1.

Analysis of risk factors for MRSA carriage among patients at admission in the surgery wards of a limited-resource hospital in Indonesia

Risk factors	No. of subjects (%)		Multivariate analysis (backward LR)
	MRSA (+) (N = 65)	MRSA (−) (N = 132)	OR	95% CI	P
Age (years)*
< 18	6 (9.2)	18 (13.6)
19–59	51 (78.5)	101 (76.5)
> 60	8 (12.3)	13 (9.8)
Gender*
Male	50 (76.9)	105 (79.5)
Female	15 (23.1)	27 (20.5)
Prior admission room†
Outpatient clinics	30 (46.2)	105 (79.5)	1
ICU	0 (0)	1 (0.8)	NA
Acute care unit	30 (46.2)	24 (18.2)	5.6	2.7–11.6	< 0.001
Burn unit	1 (1.5)	0 (0)	NA
Referred from other hospitals	4 (6.2)	2 (1.5)	7.7	1.2–49.1	0.030
Hospitalization within the past 12 months	18 (27.7)	15 (11.4)			NS
Surgical procedure within the past 3 months	13 (20.0)	9 (6.8)	6.7	2.3–19.4	< 0.001
Immunocompromised‡	6 (9.2)	4 (3.0)	7.3	1.6–33.9	0.011
Open skin lesions	0 (0)	7 (5.3)			NS

CI = confidence interval; ICU = intensive care unit; LR = logistic regression; MRSA = methicillin-resistant Staphylococcus aureus; NS = not significant; OR = odds ratio.

^*Univariate analysis was not significant (P > 0.2).

^†Prior admission room indicates what type of physical contact the patient had with hospitals immediately prior to admission to the general surgery wards. Almost 80% of the MRSA-negative patients had visited outpatient clinics only, whereas the majority (54%) of MRSA-positive patients had had a prior admission to a hospital.

^‡Patients with diabetes mellitus, chronic kidney disease, malignancy with either chemotherapy or radiotherapy, congestive heart disease; note that patients with human immunodeficiency virus infection or who use steroids on a regular basis were not among those enrolled in this study.

This study is the first risk factors analysis that identified four groups of patients at admission to an Indonesian hospital with an increased risk of carrying MRSA. Similar to previously published studies, patients directly referred from another hospital, immunocompromised patients, and patients that had a surgical procedure within the past 3 months before admission were more likely to be MRSA-carrying patients at admission in the surgery ward.^6,7 In contrast to other studies, we found that open skin lesions and previous hospitalization were not significantly associated with MRSA carriage at admission in this study.^7,8 Moreover, we found that patients transferred from the acute surgery unit (in the emergency suite) were more likely to carry MRSA at the time of transfer and admission to the general surgery wards. This finding suggests that patients experiencing an acute illness are at high risk of becoming colonized with MRSA during their stay in the acute surgery unit. However, further investigation is needed to explore the sources and routes of transmission of MRSA in this particular setting. The four high-risk groups detected in this study could be the target of selective screening of MRSA in Dr. Saiful Anwar Hospital, but these findings cannot be generalized for other hospitals since different geographical areas and health-care settings may yield different risk factors for patients to be MRSA positive at the time of their admission to surgery. However, when and wherever risk factor analysis for MRSA have yet to be conducted in most hospitals in Indonesia, the four high-risk population groups identified in this study could be used as surrogates for targeted screening of MRSA carriage among patients at admission. Indeed, similar studies are recommended to be conducted in other referral and district hospitals in Indonesia to detect additional risk factors that were not identified in this study. Patients referred from secondary care district hospitals had the highest chance to be MRSA carrier at admission in our referral hospital. However, the presence and spread of MRSA in the second-tier hospitals in Indonesia has not yet been investigated and published. Therefore, developing a network of infection control and antibiotic stewardship programs between secondary and tertiary care hospitals is needed to control MRSA in the Indonesian health-care system. In addition, it is evidently necessary to gain more insight into the epidemiology of MRSA in the secondary care hospitals to design effective targeted intervention measures for controlling MRSA in Indonesia.

Statistical analysis revealed selective screening based on the four risk factors would have a sensitivity and specificity to detect MRSA carriage at admission to the surgery wards of 72.3% and 71.3%, respectively. Only 53/197 (26.9%) patients had one or more of the risk factors, thus eliminating most patients from those that need to be screened. Including additional risk factors such as antibiotic use within the past 6 months, the use of medical devices, and contact with a known MRSA carrier may further increase the sensitivity rate. Although further risk factors analysis is needed, we have identified the high-risk populations who should be screened for MRSA carriage at admission to surgery wards. By detecting MRSA carriers on admission, barrier nursing and decolonization therapy can be applied to prevent hospital-acquired MRSA infections in these patients and to prevent the cross contamination of pathogenic MRSA to other patients, to hospital personnel, and to the innate environment of the hospital.

This study has some limitations. First, we did not include the use of medical devices, previous contact with an MRSA carrier, and previous antibiotic therapy in the risk factor analysis. Consequently, such potential risk factors on MRSA carriage could not be identified. Second, the high-risk population groups identified in this study was limited to the surgery ward with relatively small number of patients involved. Further investigation for other wards is required to discover risk factors of MRSA carriage among patients at admission to most or all wards of the entire hospital. Third, a cost-effective analysis of the proposed targeted screening in this limited-resource hospital was not carried out.

In summary, we found that patients referred from other hospitals, patients transferred from the surgical acute care unit, patients that had a surgical procedure within 3 months before admission, and immunocompromised patients were at increased risk of carrying MRSA at admission to the surgery ward in a tertiary care hospital in Indonesia. Selective screening for MRSA carriage at admission of these high-risk groups would be an efficient strategy to significantly reduce the prevalence of either MRSA colonization or infection in resource-limited hospitals. The early detection of MRSA carriage among patients at admission is important for infection prevention and control purposes.