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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 62:1152-1156 (2007)
© 2007 The Gerontological Society of America

Risk Factors for Methicillin-Resistant Staphylococcus aureus Colonization in a Geriatric Rehabilitation Hospital

Efraim Aizen, Zlata Ljubuncic, Predrag Ljubuncic, Ira Aizen and Israel Potasman

1 Fliman Geriatric Rehabilitation Hospital, Haifa.
2 The Infectious Diseases Unit, Bnai-Zion Medical Center, Haifa.
3 Bruce Rappaport Faculty of Medicine, Technion - Institute of Technology, Haifa, Israel.

Address correspondence to Efraim Aizen, MD, Fliman Geriatric RehabilitationHospital, Zalman Shneur St., PO Box 2263, Haifa 31021, Israel. E-mail: eaizen_il{at}yahoo.com


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Background. Knowledge of the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) colonization, and the frequency of transmission is vital for the implementation of MRSA infection control measures in hospitals. We assessed risk factors for and rates of colonization of MRSA upon admission to a geriatric rehabilitation hospital, and studied the contribution of the colonization on hospital mortality.

Methods. This was a prospective study conducted over a 6-month period. All patients were screened at admission, using nasal and throat swabs. Whenever necessary, blood, sputum, urine, or wound cultures were obtained. Data collected on admission included age, sex, functional status, reasons for admission to the rehabilitation unit, previous hospitalizations, known carriage or infection with MRSA in previous hospitalizations, underlying diseases, prescribed antibiotics in previous hospitalization, serum albumin, creatinine clearance, and patient management data. Risk factors for MRSA carriage on admission were estimated by using multivariate analysis.

Results. Of the 337 patients admitted during the study period, 24 (7.1%) had a MRSA isolate, and 87.4% of these were detected through screening specimens only. Of the 24 positive admissions with MRSA, 23 (95.8%) were newly identified MRSA carriers. In the multivariate analysis, the following variables were highly associated with MRSA carriage: presence of tracheotomy (p =.0001), hospitalization for deconditioning (p =.007), renal failure (p =.039), and quinolone use prior to hospitalization (p =.037). The morbidity associated with MRSA was very low, and length of stay was not influenced by carriage.

Conclusion. The prevalence of MRSA carriage on admission to geriatric rehabilitation hospitals is high. Screening on admission is probably useful, as it detects almost all MRSA carriers. However, given the low morbidity associated with MRSA observed in this study, eradication of the MRSA carrier state is questionable. Further studies are needed to determine the usefulness and cost/benefit ratio of screening.

METHICILLIN-resistant Staphylococcus aureus (MRSA) infection carries a considerable rate of morbidity and mortality in older patients. This pathogen is the second most common cause of nosocomial infections among hospitalized older adults (1). Only recently has the magnitude of asymptomatic colonization and symptomatic infection with MRSA in older patients been recognized and explored (2). Among the principal factors that have been shown to increase a patient's risk of colonization with MRSA, one may find prior hospitalization, recent use of broad-spectrum antimicrobials, impaired functional status, use of medical devices (urinary catheter, nasogastric tube, or IV catheter), and chronic diseases leading to wounds or skin breakdown (3–5). Once colonized, older patients often carry the same strain of MRSA for 3 month to 3 years (3).

Asymptomatic colonization with MRSA is an important risk factor for development of MRSA infection (4). The issues concerning what control measures are necessary and reasonable to prevent the introduction and spread of MRSA are controversial. In contrast to acute-care hospitals, where 30%–60% of colonized patients will develop a nosocomial MRSA infection, only 5%–15% of colonized residents in long-term care facilities (LTCF) will develop infection (4,6).

In 1994, the MRSA Task Force of the American Hospital Association published recommendations for the control of MRSA in acute care hospitals and in LTCFs (7). The recommendations further stressed the need for each individual facility to develop an MRSA control plan based on prevalence of MRSA in the facility and referring institutions, frequency of MRSA transmission, and availability of resources.

No group had prospectively investigated MRSA colonization and infection in a geriatric rehabilitation hospital. Knowledge of the prevalence of MRSA colonization and infection and the frequency of transmission is vital for the implementation of MRSA infection control measures in such hospitals. We assume that modes of MRSA transmission in such hospitals are different from those in LTCFs and in acute-care hospitals. We aimed to assess the prevalence and incidence of MRSA colonization over a 6-month period in a geriatric rehabilitation hospital. Patterns of MRSA acquisition within the facility were assessed, and the risk for infection in patients colonized with MRSA was studied.


   METHODS
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 Abstract
 Methods
Results
 Discussion
 References
 
Setting and Patients
The study was conducted over a 6-month period at the Fliman Rehabilitation Geriatric Hospital (a public geriatric facility affiliated with the Technion University Medical School and located in Haifa, Israel). This 150-bed geriatric rehabilitation and subacute care center offers two services: the subacute wards (50 beds) and the geriatric rehabilitation wards (100 beds). The center admits approximately 1750 patients per year. Over the past year, approximately 75% of the patients were admitted from wards in other hospitals, 15% were admitted from general hospital emergency rooms, 7% were admitted directly from nursing homes, and only 3% were admitted from home. All patients admitted to the hospital during the study period were included in the study.

Sampling
The screening program included collection of nasal, throat, and urine samples from each patient admitted to the rehabilitation wards. Samples were taken within 48 hours of admission. In addition, all skin wounds and gastrostomy and tracheotomy sites were swabbed at admission. Clinical diagnostic samples from the patients were submitted to the microbiology laboratory whenever a clinical site was suspected of infection.

Microbiological Methods
Swabs were inoculated onto selective blood agar containing phenyl ethyl alcohol (PD 042; HY Labs, Rehovot, Israel). Plates were examined for Staphylococci after 24 and 48 hours. Microbiological methods for identification of S. aureus included Gram stain, growth on sheep blood agar, and Staphylase Test (Oxoid, Basingstoke, Hampshire, U.K.). The antibiotic susceptibility pattern was determined using Mueller–Hinton agar plates supplemented with oxacillin incubated for 24 hours at 30°–35°C. S. aureus strains with oxacillin inhibition corresponding to minimum inhibitory concentration (MIC) > 2 mg/L were classified as MRSA. All MRSA isolates were recorded, together with date of sampling, sample type, name, location of the patient, and antibiotic susceptibility results.

Definitions
A carrier was defined as a patient from whom MRSA was recovered from any screening sample, in the absence of MRSA from a clinical diagnostic sample. Colonization was defined as recovery of MRSA from a clinical diagnostic sample without systemic signs of sepsis or local overt infection (8). For the purpose of this analysis, carriers and colonized patients were grouped together (MRSA cases). Infection was defined as recovery of MRSA from a clinical diagnostic sample with the presence of systemic signs of sepsis or local infection.

Data Collection
Data collection was coordinated by a physician and the epidemiological nurse of the hospital. The physician completed standardized forms for each included patient.

Data were recorded for the following variables: age, sex, functional status [the Katz Index of Activities of Daily Living was used as the functional status staging tool (9), and the cutoff value used was dependence in at least two functions], previous hospitalizations, carriage and colonization or infection with MRSA in previous hospitalization, dates of admission and discharge, underlying diseases, prescribed antibiotics, albumin, creatinine clearance (CCr; calculated using the Cockroft–Gault formula), patient management data at admission and during hospitalization, and reasons for admission to the rehabilitation unit. Reasons for rehabilitation were grouped into one of four subgroups: (i) stroke rehabilitation, (ii) rehabilitation after an orthopedic surgery, (iii) other postoperative rehabilitation (e.g., abdominal, neurosurgery), and (iv) physical deconditioning (decline in functional status usually after prolonged hospital stay).

Statistical Analysis
Statistical analysis was performed by using parametric or nonparametric tests where appropriate. Logistic regression analysis was used to identify independent predictors of colonization with MRSA at the time of admission to the rehabilitation unit as well as clinical conditions associated with the development of symptomatic MRSA infection. Data were analyzed using SPSS (Statistical Package for the Social Sciences, version 12.0; Faculty of Medicine, Technion, Haifa, Israel). Association between factors and MRSA colonization was analyzed using the chi-square test or Fisher's exact test as appropriate. Two-tailed p values of ≤.05 were considered as statistically significant.


   RESULTS
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 Abstract
 Methods
 Results
Discussion
 References
 
During the 6-month study period, 337 admissions were recorded in the four rehabilitation wards: 136 patients (40.4%) were hospitalized for stroke rehabilitation, 120 (35.6%) for rehabilitation after an orthopedic surgery, 26 (7.7%) were other postoperative (abdominal and neurosurgery) rehabilitation patients, and 55 (16.3%) were hospitalized due to physical deconditioning. Of the 337 admissions, 329 were admitted directly from other hospitals, 7 from home, and only 1 patient was admitted from a nursing home. The mean age of the 169 men and 168 women was 74.3 ± 10.9 years. Mean duration of stay at our institution was 31.3 ± 15.9 days; most patients (262) were discharged home, 25 were discharged to a nursing home, 45 were transferred to a general hospital, and 5 patients (1.5%) died.

Of the 337 admissions, 24 (7.12%) had positive test results for MRSA. This prevalence of MRSA carriage varied across subgroups of patients: It was 16.3% among patients hospitalized due to physical deconditioning, 11.5% among other postoperative rehabilitation patients, 6.6% among patients hospitalized for rehabilitation after an orthopedic surgery, and 2.9% among stroke rehabilitation patients. In only one patient (4.2%) of the 24 admissions with positive screening test results, MRSA carriage had also been detected before admission. Therefore, in 23 admissions (95.8%), MRSA carriage was newly identified by screening at admission. As shown in Table 1, nasal swabs were the most efficient way to diagnose carriage (positive in 58.3% of the 24 MRSA-positive admissions, compared to only 29.1% of throat swabs and 29.1% of swabs from clinical specimens).


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  		Table 1. Frequency of Specimens Positive for Methicillin-Resistant Staphylococcus aureus (MRSA) Carriage at Admission to Rehabilitation Ward.

 
Variables Associated With MRSA Carriage
Of the 337 admissions, 314 (93.2%) were from four neighboring general hospitals. The prevalence of MRSA carriage was significantly different between patients transferred from different hospitals. The prevalence of MRSA carriage varied across hospitals from 3.9% to 15.6%. The prevalence of MRSA carriage was significantly higher in patients admitted from one hospital (Hospital N) (5/32 or 15.6%) (p =.0447).

In addition, the univariate analysis revealed that MRSA carriage was associated with the presence of pressure ulcer on admission, presence of tracheotomy on admission, hypoalbuminemia, renal failure (CCr < 60), and deconditioning as a reason of hospitalization. Among antibiotics, quinolones were the only group associated with MRSA carriage (Table 2). Logistic regression modeling identified the presence of tracheotomy at admission, renal failure, hospitalization for deconditioning, and quinolone use to be highly and independently associated with MRSA carriage (Table 3).


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  		Table 2. Variables Associated in Univariate Analysis With Methicillin-Resistant Staphylococcus aureus (MRSA) Carriage in 337 Admitted Patients.

 

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  		Table 3. Variables Associated With Methicillin-Resistant Staphylococcus aureus Carriage on Admission to Rehabilitation, in Multivariate Analysis.

 
Definition of MRSA strains isolated in our study as community-associated (CA-MRSA) or health care–associated MRSA (HA-MRSA) was not done. Definition cannot be done only by microbiological characterization of the two types of MRSA. HA-MRSA is usually defined as a cultured MRSA infection documented more than 48 hours after admission to a hospital. According to the antibiogram obtained (Table 4), MRSA isolates were probably HA-MRSA.


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  		Table 4. Antibiotic Sensitivity of 28 Clinical Isolates of Methicillin-Resistant Staphylococcus aureus.

 

   DISCUSSION
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 Abstract
 Methods
 Results
 Discussion
References
 
Our results confirm a high prevalence of MRSA carriage at geriatric rehabilitation admission. The 7.1% prevalence found in this study is slightly lower than that in an earlier report by Manian and colleagues (10), who looked at routine screening for MRSA on admission to a general acute rehabilitation unit and reported a 12% isolation rate. We found substantial variations, however, across subgroups of rehabilitation patients. The highest isolation rate in our study was in postoperative (abdominal and neurosurgery) rehabilitation patients (11.5%) and in elderly patients hospitalized due to physical deconditioning (16.3%). We assume that this finding is related to the different incidence of MRSA colonization in the wards from which patients were transferred to the rehabilitation wards. Epidemiological data suggested that intensive care units and surgical wards are the places where most patients became colonized with MRSA. In these wards, prevalence of MRSA at discharge may reach 27% (11,12).

Our data suggest that combining nasal samples, clinical specimens, and routine throat samples ensures detection of most MRSA carriers. We found that cultures of the nares were positive in 58.3% of admissions with MRSA carriage, and that combining nasal and throat cultures allowed the detection of 87.4% of admissions with MRSA carriage. Nasal, throat, and clinical samples in combination allowed the detection of 91.7%.

We, as others investigators who looked for risk factors for MRSA carriage in hospitals (13,14), found that the presence of pressure ulcers was significantly associated with MRSA carriage in patients admitted to our geriatric rehabilitation wards. This result is not surprising, as presence of pressure ulcers is probably a marker for intensive prolonged medical care and, consequently, for frequent opportunities for MRSA acquisition. There is a well-established association between presence of pressure ulcers and persistent MRSA carriage in hospitalized patients (15).

We, as others, confirm that recent use of broad-spectrum antimicrobials increases a patient's risk of colonization following exposure to MRSA (3,5). Although recent use of antimicrobials was found in the univariate analysis to be associated with MRSA carriage (p =.006), this finding was not significant after adjustment in the regression analysis (p =.077). The finding that quinolones were the only group of antibiotics associated with MRSA carriage is interesting. This observation is consistent with the results of other studies linking fluoroquinolone use to resistance MRSA (16). A recent study also showed significant associations between a hospital's volume of fluoroquinolone use and percent resistance (17).

Our finding that, among all patients admitted to our hospital, presence of a tracheotomy was the strongest risk factor (odds ratio = 25.2) for MRSA carriage is very interesting. We did not find in the literature other studies that demonstrated such a connection. Our finding would require confirmation in a larger study of tracheotomy patients, because there are only nine tracheotomy patients in our study. The use of medical devices such as a urinary catheter, nasogastric feeding tube, or IV catheter has been shown to increase the risk of MRSA colonization in elderly patients (3,5). We believe that the high rate of MRSA carriage among patients with a tracheotomy is apparently related to the intensive and prolonged hospitalization that these patients experienced and, consequently, to the frequent opportunities for MRSA acquisition.

Renal failure and hypoalbuminemia were also associated with MRSA carriage on admission, as independent risk factors. It is not clear why these factors were associated with MRSA carriage. Renal failure and hypoalbumunemia might be markers for other risk factors for MRSA acquisition or persistence not collected in our study. However, hypoalbuminemia is a common condition in patients with serious illness, and is correlated with increased morbidity and mortality and prolonged stays in hospitals and intensive care units (ICUs) (18). Malnutrition is common in patients with severe renal failure, and hypoalbuminemia is highly predictive of future mortality risk in patients with renal failure (19).

Whether MRSA screening at geriatric rehabilitation admission is worthwhile remains a matter of debate. Most recommendations for controlling the spread of MRSA include screening at hospital admission of most patients or selected patients according to the epidemiological conditions (20,21). Other recommendations do not include MRSA screening at admission, as this strategy might be expensive and has not been proven in controlled studies to decrease the incidence of MRSA (22). In our study, only 4.2% of cases of MRSA carriage at rehabilitation ward admission were known previously, and none of the cases were associated with positive clinical samples during the stay in the ward. Therefore, screening tests at admission elicited all positive test results for MRSA carriers. This very high proportion can be ascribed to restriction of screening of patients considered at high risk of MRSA carriage in the wards from which patients were transferred to the rehabilitation wards before discharge.

We did not attempt to eradicate MRSA colonization in our hospital but rather sought to determine the prevalence of colonization and the risk of infection in colonized patients. On the basis of our results, we should be able to design appropriate control measures for a geriatric rehabilitation hospital. Screening identified all positive MRSA carriers on admission to our hospital. Despite these plausible figures, the direct effect of MRSA carriage in our hospital appears to be limited, given the low rate of associated morbidity. We believe that, given that patients are continuously transferred between rehabilitation hospitals and acute-care facilities, it is reasonable to consider rehabilitation units together with all other care units and to measure the effect of MRSA on a regional health care network, rather than on a given ward or hospital. The relationship between rates of MRSA carriage and the difference in patients and facility profile is demonstrated by the high rate (15.6%) of admissions positive for MRSA among patients coming from a specific hospital (hospital N). Hospital N is a 609-bed general hospital. The spectrum of patients sent to rehabilitation from this hospital was very similar to that of patients from the other hospitals. Although we found no publication from this hospital regarding higher rates of MRSA or outbreaks of MRSA, we may assume that this finding is related to a high percentage of MRSA carriage in this institution. Transfer of patients between hospitals is the second most important way of increasing the risk of MRSA in a given hospital (23).

The identification of all reservoirs (colonized or infected patients and simple carriers) within wards is considered to be a major component of all control programs (7,13), and isolation strategies recommended to prevent cross-transmission may be hindered if carriers are not identified upon admission. The usefulness and cost/benefit ratio of the collection of samples for screening remain open to debate (7,15). Whether the eradication of the MRSA carrier state in patients in a geriatric rehabilitation facility will lead to a decreased rate of MRSA infection in the hospital has yet to be documented. In contrast to general hospitals, where MRSA colonization on admission to the hospital increases the risk for later MRSA infection, we found no such increase in our geriatric rehabilitation hospital. Given the low morbidity associated with MRSA observed in our hospital, this examination is questionable. Perhaps only the patients at greater risk for infection, if identified, should be treated.

Conclusion
Screening for MRSA at geriatric rehabilitation admission is probably useful, as it detects almost all MRSA carriers. Screening at admission should include nasal swabs and sampling of the throat, in addition to collection of clinical specimens. Factors associated with MRSA carriage at geriatric rehabilitation admission are presence of pressure ulcer, presence of tracheotomy, hypoalbuminemia, renal failure, antibiotic use prior to hospitalization, and hospitalization for deconditioning. Further studies are needed to determine the usefulness and cost/benefit ratio of the collection of samples for screening.


   Footnotes
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 Abstract
 Methods
 Results
 Discussion
 References
 
Decision Editor: Luigi Ferrucci, MD, PhD

Received August 3, 2006

Accepted December 29, 2006


   References
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 Abstract
 Methods
 Results
 Discussion
 References
 

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