Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) is a significant cause of health care–associated infection. The overall effectiveness of surveillance screening programs is not well established. A retrospective cohort study was performed to evaluate the impact of a surveillance screening program on the rates of health care–associated MRSA infection (HA-MRSA-I) at a single institution. A subset of surgical patients was analyzed separately. Multivariate regression techniques were used to identify predictors of the desired outcomes. The overall MRSA infection rate was 1.3% in the before cohort and 3.2% in the after cohort. After excluding patients with a history of MRSA infection or MRSA colonization, HA-MRSA-I decreased from 1.2% to 0.87%. There was a similar overall increase in the surgical group, 1.4% to 2.3%, and decrease in HA-MRSA-I, 1.4% to 1.0% (P < 0.001). For all patients, surgery, African American race, and increased length of stay conferred an increased likelihood of HA-MRSA-I. Females and patients in the after cohort had a lower risk of HA-MRSA-I (P < 0.01). In the after cohort, the results were similar, with surgery, African American race, and length of stay associated with an increased risk, and female sex associated with a decreased risk (P < 0.05). African American race and increased age had a higher likelihood of screening positive for MRSA colonization, while the surgical group, females, and Hispanic patients were less likely (P < 0.05). HA-MRSA-I was associated with a higher mortality among all patients (P < 0.001). Mortality rates were similar with HA-MRSA-I for all patients (10.8% vs 9.5%, P = 0.55) and in the surgical group (8.3% vs 6.8%, P = 0.58). In conclusion, surveillance programs may be effective in decreasing HA-MRSA-I. Further studies are needed to determine how to reduce transmission, particularly among African Americans and those with increased lengths of stay.
Methicillin-resistant Staphylococcus aureus (MRSA) is a significant cause of health care–associated infection (1) and is associated with increased hospital mortality (2, 3). In addition, MRSA is the leading cause of surgical site infection (4, 5). In 2003, the Society of Healthcare Epidemiology of America released guidelines strongly supporting the use of active surveillance cultures and contact isolation programs (6). A decrease in overall health care–associated MRSA infections (HA-MRSA-I) has since been demonstrated across a wide range of clinical and geographical settings in the United States (7). Surveillance programs have also proven to be effective in MRSA outbreaks in the intensive care unit (ICU) setting (8). Despite a decrease in overall HA-MRSA-I rates after implementation of active surveillance culture programs, the effect of HA-MRSA-I rates on specific patient populations, including patients undergoing invasive surgical procedures, is not well established (9, 10).
The purpose of this study was to evaluate rates of HA-MRSA-I before and after implementation of a hospitalwide screening program at a large teaching hospital with a high surgical volume. We examined the effect of this infection control initiative in the overall hospital population as well as for patients undergoing a wide range of common surgical procedures among a variety of specialties. We hypothesized that rates of HA-MRSA-I would decrease after implementation of a screening program, both hospitalwide and for patients undergoing surgical procedures.
METHODS
This institutional review board–approved retrospective cohort study took place at Baylor University Medical Center at Dallas, a 1000-bed academic medical center and level I trauma center in a large metropolitan area. Our current practice involves performing nasal swab MRSA polymerase chain reaction (PCR) screens on all patients who meet one of the following screening criteria: a prior history of MRSA colonization or infection (patient is placed in contact isolation); hospitalization within the preceding year; transfer from an extended care facility; presence of open or draining skin wounds (patient is placed in contact isolation); current admission to ICU; or current hemodialysis. Standard barrier and isolation precautions, including gown and gloves, are applied to all patients with a positive screen. With the exception of several four-bed pods in the surgical intensive care unit, all rooms are single rooms.
A hospitalwide MRSA surveillance program was implemented in January 2009. Prior to this initiative, standard barrier and isolation practices were implemented only if patients had a documented MRSA infection or if the patient or patient's history indicated prior MRSA infection. For purposes of this study, the term “MRSA infection” is used if a positive MRSA culture was obtained on a patient from any source. The term “positive screen” is used for patients who had a positive nasal PCR screen denoting MRSA colonization, but not an active MRSA infection.
All inpatient hospital admissions from October 1st to September 30th for 2007 to 2008 (before cohort) and 2010 to 2011 (after cohort) were analyzed. The 12-month interval between cohorts was included to allow full implementation across all units of the hospital. All patients in the after cohort underwent nasal MRSA PCR screening under the criteria mentioned above. Patients with a previous MRSA infection, as well as those readmitted with a previous positive screen for MRSA, were excluded. Patients who initially screened negative and subsequently developed an MRSA infection were considered to have HA-MRSA-I. A subset of patients undergoing a wide array of surgical procedures across multiple specialties in the before and after cohort were analyzed separately. These included general surgical, gynecologic, orthopedic, cardiothoracic, transplant, oral-maxillofacial, plastics, and urologic procedures. International Classification of Diseases, Clinical Modification, ninth revision (ICD-9) procedure codes were used to identify procedures by those specialties. Procedures were included in the analysis if at least 50 were performed during the study period. Logistic regression analysis was performed to determine which factors contributed to predicting HA-MRSA-I and how HA-MRSA-I affected patient mortality. P values < 0.05 were considered significant.
Our primary endpoint was the incidence of HA-MRSA-I. The secondary endpoint was the impact of HA-MRSA-I on patient mortality. Multivariate regression techniques were used to elucidate predictors of these outcomes.
RESULTS
There were 36,244 patients in the before cohort, of whom 16,740 underwent a surgical procedure, and 36,068 in the after cohort, of whom 15,044 underwent a surgical procedure. Patient characteristics are shown in Tables 1 and 2.
Table 1.
Patient characteristics for all patients and patients in the surgical group
| Combined | Before | After | |
|---|---|---|---|
| All patients | |||
| N | 72,312 | 36,244 | 36,068 |
| Age at admit, mean ± SD (years) | 54.2 ± 19.2 | 54.1 ± 19.1 | 54.2 ± 19.3 |
| Male | 29,465 (41%) | 15,020 (41%) | 14,445 (40%) |
| Female | 42,837 (59%) | 21,216 (59%) | 21,621 (60%) |
| Race | |||
| White | 43,215 (60%) | 22,609 (63%) | 20,606 (57%) |
| African American | 18,473 (26%) | 8,712 (24%) | 9,761 (27%) |
| Hispanic | 8,324 (12%) | 3,770 (10.5) | 4,554 (12.7%) |
| Asian | 705 (1%) | 289 (0.8%) | 416 (1.2%) |
| Other | 1047 (1.5%) | 431 (1.2%) | 616 (1.7%) |
| Length of stay, median (IQR) (days) | 3.8 (2.3, 6.8) | 3.8 (2.2, 6.8) | 3.8 (2.3, 6.9) |
| Discharged alive | 69.761 (97%) | 34,917 (96%) | 34,844 (97%) |
| Died | 2,551 (4%) | 1,327 (4%) | 1,224 (3%) |
| Surgical group | |||
| N | 31,784 | 16,740 | 15,044 |
| Age at admit, mean ± SD (years) | 50.7 ± 18.5 | 51.1 ± 18.2 | 50.3 ± 18.8 |
| Male | 11,667 (37%) | 6,416 (38%) | 5,251 (35%) |
| Female | 20,109 (63%) | 10,317 (62%) | 9,792 (65%) |
| Race | |||
| White | 21,021 (67%) | 11,460 (70%) | 9,561 (64%) |
| African American | 5,820 (19%) | 2,901 (18%) | 2,919 (20%) |
| Hispanic | 3,705 (12%) | 1,727 (11%) | 1,978 (13%) |
| Asian | 373 (1.2%) | 151 (1%) | 222 (1.5%) |
| Other | 473 (1.5%) | 183 (1.1%) | 290 (2%) |
| Length of stay, median (IQR) (days) | 3.6 (2.3, 6.8) | 3.7 (2.3, 6.7) | 3.5 (2.3, 6.9) |
| Discharged alive | 31,239 (98%) | 16,430 (98%) | 14,809 (98%) |
| Died | 545 (1.7%) | 310 (2%) | 235 (2%) |
SD indicates standard deviation; IQR, interquartile range.
Table 2.
Comparison of surgical versus nonsurgical patients
| Variable | Surgical (N = 31,784) | Nonsurgical (N = 40,528) | P value |
|---|---|---|---|
| Age at admit, mean ± SD (years) | 50.7 ± 18.5 | 56.9 ± 19.3 | < .0001 |
| Male | 11,667 (37%) | 17,798 (44%) | |
| Female | 20,109 (63%) | 22,728 (56%) | < .0001 |
| Race | |||
| White | 21,021 (67%) | 22,194 (55%) | |
| African American | 5,820 (19%) | 12,653 (31%) | |
| Hispanic | 3,705 (12%) | 4,619 (11%) | |
| Asian | 373 (1.2%) | 332 (0.8%) | |
| Other | 473 (1.5%) | 574 (1.4%) | < .0001 |
| Length of stay, median (IQR) (days) | 3.6 (2.3, 6.8) | 3.9 (2.2, 6.8) | < .0001 |
| Discharged alive | 31,239 (98%) | 38,522 (95%) | |
| Died | 545 (1.7%) | 2006 (5%) | < .0001 |
SD indicates standard deviation; IQR, interquartile range.
The overall MRSA infection rate was 1.3% (453 patients) in the before cohort and 3.2% (1136 patients) in the after cohort (P < 0.001). When patients with previous MRSA infection or colonization were excluded, those with HA-MRSA-I decreased from 1.2% to 0.87% (Table 3). Similarly, there was an increase in the rate of overall MRSA infection in the surgical group, from 1.4% to 2.3%, along with a decrease in HA-MRSA-I, from 1.4% to 1.0% (Table 3).
Table 3.
MRSA infection rates for patients in both cohorts
| Cohort | Infection | Time | Yes | No | P value |
|---|---|---|---|---|---|
| All | All positive cultures | Before | 453 (1.3%) | 35,791 (98.8%) | |
| After | 1136 (3.2%) | 34,932 (96.9%) | <.001 | ||
| Only HA-MRSA-I | Before | 426 (1.2%) | 35,791 (98.8%) | ||
| After | 307 (0.87%) | 34,932 (99.1%) | <.001 | ||
| Surgical | All positive cultures | Before | 236 (1.4%) | 16,504 (98.6%) | |
| After | 345 (2.3%) | 14,699 (97.7%) | <.001 | ||
| Only HA-MRSA-I | Before | 229 (1.4%) | 16,504 (98.6%) | ||
| After | 148 (1.0%) | 14,699 (99.0%) | 0.002 |
HA-MRSA-I indicates health care–associated methicillin-resistant Staphylococcus aureus infection.
For the total patient population, including both before and after cohorts, patients in the surgical group, African Americans, and patients with an increased length of stay had an increased likelihood of developing HA-MRSA-I. Female patients and patients in the after cohort were less likely to develop HA-MRSA-I (Table 4). When only patients in the after cohort were analyzed, the results were similar, with surgery, African American race, and length of stay associated with an increased risk of HA-MRSA-I, and female sex associated with a decreased risk (Table 4).
Table 4.
Factors associated with health care–associated methicillin-resistant Staphylococcus aureus infection
| Category | Variable | Odds ratio | 95% CI | P value |
|---|---|---|---|---|
| In all patients | ||||
| Cohort | Before | — | ||
| After | 0.73 | (0.63, 0.85) | < .001 | |
| Surgery | No (referent) | — | ||
| Yes | 1.3 | (1.12, 1.51) | < .001 | |
| Age | 1 | (1.00, 1.01) | 0.07 | |
| Sex | Male (referent) | — | ||
| Female | 0.56 | (0.48, 0.65) | < .001 | |
| Race | White (referent) | — | ||
| African American | 1.31 | (1.1, 1.55) | 0.002 | |
| Hispanic | 0.99 | (0.77, 1.28) | 0.15 | |
| Asian | 0.29 | (0.07, 1.18) | 0.10 | |
| Other | 0.65 | (0.31, 1.38) | 0.65 | |
| Length of stay | 1.05 | (1.05, 1.06) | < .001 | |
| In the after cohort | ||||
| Surgery | No (referent) | — | ||
| Yes | 1.33 | (1.05, 1.70) | < .0167 | |
| Age | 1.00 | (1.0, 1.01) | 0.3334 | |
| Sex | Male (referent) | — | ||
| Female | 0.49 | (0.39, 0.62) | < .0001 | |
| Race | White (referent) | — | ||
| African American | 1.48 | (1.45, 1.91) | 0.0212 | |
| Hispanic | 1.00 | (0.69, 1.47) | 0.7821 | |
| Asian | 0.69 | (0.17, 2.79) | 0.5864 | |
| Other | 0.73 | (0.27, 1.98) | 0.5479 | |
| Length of stay | 1.05 | (1.03, 1.04) | < .0001 |
With regards to the likelihood of screening positive for MRSA colonization, African American race and increased age were associated with a higher likelihood of screening positive, while patients in the surgical group, female patients, and Hispanic patients were less likely to screen positive (Table 5). HA-MRSA-I was associated with a higher mortality for both the entire patient population and surgical group in both cohorts (Table 5). There was no significant difference in the overall mortality of patients with HA-MRSA-I for all patients (10.8% vs 9.5%, P = 0.55) as well as the surgical group (8.3% vs 6.8%, P = 0.58).
Table 5.
Odds ratio of screening positive for MRSA colonization and of death for patients with health care–associated MRSA infection
| Category | Variable | Odds ratio | 95% CI | P value |
|---|---|---|---|---|
| Screening positive for MRSA colonization | ||||
| Surgery | No (referent) | |||
| Yes | 0.53 | (0.45, 0.62) | < .0001 | |
| Age | 1.02 | (1.02, 1.03) | < .0001 | |
| Sex | Male (referent) | — | ||
| Female | 0.77 | (0.67, 0.89) | 0.0003 | |
| Race | White (referent) | — | ||
| African American | 1.41 | (1.21, 1.64) | 0.0312 | |
| Hispanic | 0.70 | (0.53, 0.92) | 0.0003 | |
| Asian | 1.50 | (0.81, 2.76) | 0.2783 | |
| Other | 1.31 | (0.79, 2.17) | 0.5250 | |
| Death for patients with health care–associated MRSA infection | ||||
| All patients | Before | 3.27 | (2.40, 4.46) | < .0001 |
| After | 3.12 | (2.12, 4.60) | < .0001 | |
| Surgical patients | Before | 5.06 | (3.12, 8.21) | < .0001 |
| After | 4.84 | (2.51, 9.32) | < .0001 |
MRSA indicates methicillin-resistant Staphylococcus aureus.
DISCUSSION
Our data indicate that the overall MRSA infection rate increased during the study period for the entire patient population as well as for patients in the surgical group. This occurred despite implementation of the screening program. This is consistent with an overall increase in community-acquired MRSA infections, which Mera and colleagues demonstrated as an increase from 22.3% in 1998 to 66.1% in 2007 (11). The purpose of the MRSA screening program is to protect patients without previous colonization from acquiring an MRSA infection while in the hospital (HA-MRSA-I). While the desired outcome is to decrease MRSA infection rates hospitalwide, surveillance programs can also have a positive impact on HA-MRSA-I, despite an overall increase in MRSA infection rate.
When excluding patients with a history of MRSA infection or MRSA colonization, the overall HA-MRSA-I rate decreased by 27.5% for the overall patient population and 28.6% for the patients in the surgery group. Patients with MRSA nasal colonization are at a significant increased risk for the development of MRSA infections. Stenehjem and colleagues demonstrated this regardless of the quantitative burden detected on PCR screening. During their study period, 4.3% of noncarriers developed a MRSA infection compared with 18.5% and 17.2% of low- and high-burden patients, respectively (12).
Previous studies have demonstrated a greater than twofold increased incidence of MRSA infections among African Americans, 66.5 per 100,000, versus the standardized incidence rate of 31.8 per 100,000. Male patients had slightly higher infection rates at 37.5 per 100,000, while patients older than 65 years of age had rates of 127.7 per 100,000 (13). Our study showed that African American patients and patients with increased lengths of stay were at increased risk of developing MRSA infection, and that female patients had a decreased risk. Graffunder and colleagues identified previous surgery and longer lengths of stay before infection as independent risk factors for developing MRSA infection, along with previous hospitalization, enteral feedings, and macrolide and levofloxacin use (14).
The major limitation of this study is its retrospective design. Therefore, the majority of patients with a positive screen will be in the after cohort when the policy became hospitalwide. Since these patients are known to be at increased risk of developing MRSA infection and were omitted from the final analysis by our study criteria, this could potentially create a falsely elevated rate of HA-MRSA-I in the before group. However, given the retrospective observational nature of the study, the data pertaining to the rate of nasal carriage in the before group were not available. Nonetheless, the method of documenting HA-MRSA-I is consistent between the groups. Furthermore, no data regarding compliance with the screening protocol were available for our analysis. Suboptimal compliance with hand hygiene (52%, range 27%–86%), glove use (62%, range 11%–98%), and the use of gown or other protective clothing (57%, range 8%–93%) was reported by Gammon et al (15).
Improved MRSA infection rates have been demonstrated in certain patient populations where more aggressive measures were taken than standard barrier and isolation practices. MRSA infection rates decreased by 93% in cardiac surgical wounds after a program was initiated that not only screened patients, but included additional interventions such as decolonizing hospital staff who screen positive, providing vancomycin prophylaxis for patients who screen positive, and administering mupirocin calcium nasal ointment for all patients regardless of screening status (16). MRSA infections at percutaneous gastrostomy sites decreased from 12% to 29% over a 33-month period to 2% after a screening and decontamination program was initiated. The protocol involved screening for MRSA from multiple sites, nasal treatment with mupirocin, and daily skin decontamination prior to the procedure (17). MRSA infection rates among ICU patients decreased from 3.0% to 1.5% when enhanced cleaning procedures were used in rooms previously occupied by patients with MRSA. A similar reduction in vancomycin-resistant enterococci infection rates from 3.0% to 2.2% was also demonstrated (18). However, Camus and colleagues did not show a reduction in MRSA acquisition in the ICU setting with more aggressive intervention protocols, including repeated MRSA screening, contact and droplet isolation precautions, and decontamination with nasal mupirocin and chlorhexidine body wash for MRSA-positive patients (19).
HA-MRSA-I remains a serious problem in the modern health care environment. Our study suggests that surveillance programs are effective in decreasing these infections, both hospitalwide and among surgical patients. We also confirm the increased mortality associated with HA-MRSA-I. Further studies are needed to aid in the reduction of the transmission of this disease among hospitalized patients, with particular focus on African American patients and those with increased lengths of stay.
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