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Original Contribution |

Epidemiology of Staphylococcus aureus Blood and Skin and Soft Tissue Infections in the US Military Health System, 2005-2010 FREE

Michael L. Landrum, MD; Charlotte Neumann, MPH; Courtney Cook, MS; Uzo Chukwuma, MPH; Michael W. Ellis, MD; Duane R. Hospenthal, MD, PhD; Clinton K. Murray, MD
[+] Author Affiliations

Author Affiliations: Infectious Disease Service, San Antonio Military Medical Center, Fort Sam Houston, Texas (Drs Landrum, Hospenthal, and Murray); Infectious Disease Clinical Research Program (Dr Landrum) and Division of Infectious Diseases (Dr Ellis), Uniformed Services University of the Health Sciences, Bethesda, Maryland; and EpiData Center Department, Navy and Marine Corps Public Health Center, Portsmouth, Virginia (Mss Neumann, Cook, and Chukwuma). Dr Landrum is now with Bellin Health, Green Bay, Wisconsin. Dr Hospenthal is now retired from military service.


JAMA. 2012;308(1):50-59. doi:10.1001/jama.2012.7139.
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Context Rates of hospital-onset methicillin-resistant Staphylococcus aureus (MRSA) infections are reported as decreasing, but recent rates of community-onset S aureus infections are less known.

Objectives To characterize the overall and annual incidence rates of community-onset and hospital-onset S aureus bacteremia and skin and soft tissue infections (SSTIs) in a national health care system and to evaluate trends in the incidence rates of S aureus bacteremia and SSTIs and the proportion due to MRSA.

Design, Setting, and Participants Observational study of all Department of Defense TRICARE beneficiaries from January 2005 through December 2010. Medical record databases were used to identify and classify all annual first-positive S aureus blood and wound or abscess cultures as methicillin-susceptible S aureus or MRSA, and as community-onset or hospital-onset infections (isolates collected >3 days after hospital admission).

Main Outcome Measures Unadjusted incidence rates per 100 000 person-years of observation, the proportion of infections that was due to MRSA, and annual trends for 2005 through 2010 (examined using the Spearman rank correlation test or the Mantel-Haenszel χ2 test for linear trend).

Results During 56 million person-years (nonactive duty: 47 million person-years; active duty: 9 million person-years), there were 2643 blood and 80 281 wound or abscess annual first-positive S aureus cultures. Annual incidence rates varied from 3.6 to 6.0 per 100 000 person-years for S aureus bacteremia and 122.7 to 168.9 per 100 000 person-years for S aureus SSTIs. The annual incidence rates for community-onset MRSA bacteremia decreased from 1.7 per 100 000 person-years (95% CI, 1.5-2.0 per 100 000 person-years) in 2005 to 1.2 per 100 000 person-years (95% CI, 0.9-1.4 per 100 000 person-years) in 2010 (P = .005 for trend). The annual incidence rates for hospital-onset MRSA bacteremia also decreased from 0.7 per 100 000 person-years (95% CI, 0.6-0.9 per 100 000 person-years) in 2005 to 0.4 per 100 000 person-years (95% CI, 0.3-0.5 per 100 000 person-years) in 2010 (P = .005 for trend). Concurrently, the proportion of community-onset SSTI due to MRSA peaked at 62% in 2006 before decreasing annually to 52% in 2010 (P < .001 for trend).

Conclusion In the Department of Defense population consisting of men and women of all ages from across the United States, the rates of both community-onset and hospital-onset MRSA bacteremia decreased in parallel, while the proportion of community-onset SSTIs due to MRSA has more recently declined.

Figures in this Article

The magnitude of invasive methicillin-resistant Staphylococcus aureus (MRSA) infections as well as the emergence of community-onset MRSA infections in the United States has been well documented.14 Commonly due to the pulsed-field type USA300 strain of MRSA, outbreaks of skin and soft tissue infections (SSTIs) have been observed in prisoners, athletes, and other risk groups.5,6 In parallel with the emergence of community-onset MRSA infections in the US civilian population, SSTIs have become a significant public health issue for the US military. During military training, approximately 4% to 6% of all individuals may experience an SSTI.7,8 Furthermore, S aureus has been isolated from 91% of such cases, with MRSA accounting for 70% of S aureus isolates. MRSA also has been shown to be a common cause of S aureus bacteremia and other infections in population-based studies from the United States, particularly health care–associated infections.911 However, recent studies have shown encouraging decreases in the rates of health care–associated and hospital-onset invasive MRSA infections and MRSA central line–associated infections.4,12

Most previously published studies on community-onset MRSA infections and SSTIs did not present data on methicillin-susceptible S aureus (MSSA) SSTI, evaluated 1 city or local region, or were not able to simultaneously evaluate temporal changes in both the community and hospital settings. The latter consideration is important given that (1) data suggest community-onset infections due to the USA300 strain have become an increasingly important reservoir for MRSA disease overall,13 and (2) rates of health care–associated MRSA infections may be decreasing.4,12 Therefore, more recent population-based data on the burden of S aureus disease in the community are needed. This study sought to characterize the concurrent epidemiology of S aureus (MRSA and MSSA) bacteremia and SSTIs from 2005 through 2010 in the community and hospital settings in a large population composed of individuals of all ages from all regions of the United States, using information from an integrated health care network, the US Military Health System.

Study Population

The surveillance population included all Department of Defense TRICARE beneficiaries who were eligible to receive care at a military medical treatment facility (MTF) from January 2005 through December 2010. TRICARE beneficiaries were defined as active duty members, retirees, medically eligible guard or reservists, and immediate family members of active duty members, retirees, and medically eligible guard or reservists. The Department of Defense TRICARE network is composed of 266 MTFs of varied sizes and services (predominantly primary care clinics and smaller, community-type hospitals) throughout the United States and limited locations overseas. Veterans Affairs institutions are not included. Additional information on the study population, TRICARE regions, and MTFs is provided in the eMethods. This study involving deidentified data was approved and determined to be nonhuman subjects research by the institutional review board at the San Antonio Military Medical Center.

Data Collection

Within the Department of Defense health care system, all microbiology laboratory data are recorded electronically into each MTF's Composite Health Care System. These passive surveillance data have been stored in the Composite Health Care System in the health level 7 format by the Department of Defense beginning on January 1, 2005, and used for analysis and public health surveillance purposes by the EpiData Center Department, Navy and Marine Corps Public Health Center. All microbiologically positive blood (including coagulase-negative staphylococci) and wound or abscess cultures from January 1, 2005, through December 31, 2010, were identified from health level 7 microbiology data. Culture results without microbiological growth are not captured in health level 7 data. Clinical data from each infection, including patient outcomes, were not available.

From all positive S aureus blood and wound or abscess cultures, only unique S aureus isolates, defined as the first isolate per patient per calendar year for each specimen source (blood, wound, or abscess), were included for further analysis. The number of individuals in the beneficiary population and demographic characteristics were obtained from the Military Health System Mart database. Data regarding self-reported race or ethnicity were not available for analysis.

Definitions

S aureus isolates were categorized into 1 of 2 groups according to susceptibility results for oxacillin, cefoxitin, cefazolin, and imipenem: (1) MRSA: isolates resistant to at least 1 of the listed antibiotics, or (2) MSSA: isolates sensitive to all of the above listed antibiotics that were tested.14 Community-onset infections were defined as (1) isolates collected in ambulatory clinics or emergency departments, or (2) inpatient isolates collected within the first 3 calendar days of hospital admission. Hospital-onset infections were defined as inpatient isolates collected more than 3 calendar days after admission similar to previous studies.4,15 The classification of infections as health care–associated community onset4 was not used because information on health care exposures other than hospital admission was not available.

Statistical Analyses

Characteristics of the study population and S aureus cultures were summarized with descriptive statistics. Proportions were compared with χ2 tests. Unadjusted incidence rates were used to describe the burden of S aureus bacteremia and SSTIs in the Department of Defense TRICARE beneficiary population per 100 000 person-years of observation overall and by year. The mid-year beneficiary population identified in a given calendar year was used as an estimate of the person-years for that period. Ninety-five percent confidence intervals for the unadjusted incidence rates were calculated using a normal approximation.16 We also calculated overall and annual incidence rates standardized to US population data for 2000 and adjusted for age and sex using the direct method, but because standardization and adjustment had little effect on these rates, we are primarily reporting the unadjusted rates.

To determine the relationship between infection rates and calendar year, as well as the direction and strength of the association, the Spearman rank correlation test and coefficient (rs) were used. The Mantel-Haenszel χ2 test for linear trend was used to examine trends in the proportion of infections due to S aureus or MRSA over the 6-year study period. Active duty service members encounter unique exposures affecting S aureus infection risk. Therefore, subanalyses were performed for active duty and nonactive duty beneficiaries. In all analyses, P values were 2-sided with values of less than .05 considered statistically significant. No adjustment was made for multiple comparisons. All statistical analyses were performed using SAS version 9.2 (SAS Institute Inc).

Demographic characteristics of the overall study population remained similar from 2005 through 2010 (Table 1). Nonactive duty individuals were distributed among age and sex categories, while active duty beneficiaries were predominantly 18 to 44 years of age and male (eTable 1 and eTable 2). From 2005 through 2010, there were a total of 62 326 positive blood cultures and 181 317 positive wound or abscess cultures in the Department of Defense Military Health System (Table 2). S aureus was isolated from 12% of all blood cultures and 62% of all wound or abscess cultures. The percentage of all blood and wound or abscess cultures due to S aureus and MRSA significantly decreased from 2005 through 2010 (P < .001 for trend). During this same time, more than 9.2 million people were eligible to receive care within the Department of Defense health care system each year, providing more than 56 million person-years of observation (nonactive duty: 47 million person-years; active duty: 9 million person-years). In the first year of observation (2005), 52% of individuals in the study population were men and 84% were nonactive duty.

Table Graphic Jump LocationTable 1. Demographic Characteristics of US Department of Defense TRICARE Beneficiaries, 2005-2010
Table Graphic Jump LocationTable 2. Positive Blood and Wound Abscess Cultures in TRICARE Beneficiaries

There were 2643 blood and 80 281 wound or abscess annual first-positive S aureus cultures included for further analyses (Table 3). Community-onset infections accounted for 2094 (79%) cases of S aureus bacteremia and 79 801 (99%) cases of S aureus SSTIs. MRSA represented 42% of all annual first-positive S aureus blood isolates, and 58% of all annual first-positive S aureus wound or abscess isolates.

Table Graphic Jump LocationTable 3.Staphylococcus aureus Infections by Setting, Culture Type, and Methicillin Resistance for Overall Study Population
Rates of Infection by Year and Demographic Characteristics

From 2005 through 2010, the overall unadjusted rates of S aureus were 4.7 per 100 000 person-years (95% CI, 4.5-4.9 per 100 000 person-years) for bacteremia and 142.8 per 100 000 person-years (95% CI, 141.8-143.8 per 100 000 person-years) for SSTIs. Unadjusted rates for S aureus bacteremia ranged from 3.6 to 6.0 per 100 000 person-years, whereas the unadjusted rates for S aureus SSTIs ranged from 122.7 to 168.9 per 100 000 person-years. After standardizing and adjusting for age and sex, the rate of S aureus bacteremia was 4.3 (95% CI, 4.1-4.4) and the rate of SSTI was 144.5 (95% CI, 143.5-145.5).

Community-Onset S aureus Bacteremia and SSTIs.Unadjusted rates significantly decreased for both community-onset MRSA and MSSA bacteremia from 2005 through 2010 from 1.7 per 100 000 person-years (95% CI, 1.5-2.0 per 100 000 person-years) to 1.2 per 100 000 person-years (95% CI, 0.9-1.4 per 100 000 person-years) for community-onset MRSA (rs = 0.94; P = .005 for trend), and from 2.9 per 100 000 person-years (95% CI, 2.5-3.2 per 100 000 person-years) to 1.7 per 100 000 person-years (95% CI, 1.5-2.0 per 100 000 person-years) for community-onset MSSA (rs = 0.94; P = .005 for trend; Table 3). During this same period, no significant overall trend was observed in the rate of community-onset MRSA (rs = 0.26; P = .62) or MSSA SSTIs (rs = 0.71; P = .11). In subanalyses of community-onset S aureus bacteremia and SSTIs in nonactive duty individuals, results were similar showing that the annual unadjusted rates of community-onset MRSA (P < .001) and community-onset MSSA bacteremia (P = .005) decreased significantly from 2005 through 2010, and no significant overall trends in the rates of community-onset MRSA (P = .62) or community-onset MSSA SSTIs (P = .54) were observed (Table 4). Overall and annual rates of S aureus bacteremia and SSTIs for active duty individuals are provided in eTable 3.

Table Graphic Jump LocationTable 4.Staphylococcus aureus Infections by Setting, Culture Type, and Methicillin Resistance for Nonactive Duty Study Subpopulation

In the entire study population, rates of community-onset S aureus bacteremia varied by demographic characteristics (Table 5). The rate of community-onset MRSA bacteremia was highest for those aged 65 years or older (3.1 per 100 000 person-years [95% CI, 2.8-3.5 per 100 000 person-years]), whereas the rates of community-onset MSSA bacteremia were highest in those aged 4 years or younger (4.5 per 100 000 person-years [95% CI, 3.8-5.2 per 100 000 person-years]) and aged 65 years or older (3.4 per 100 000 person-years [95% CI, 3.1-3.8 per 100 000 person-years]).

Table Graphic Jump LocationTable 5. Community-Onset Staphylococcus aureus Infections for Overall Study Population

The rates of community-onset bacteremia also were higher in men (MRSA: 1.8 per 100 000 person-years [95% CI, 1.7-2.0 per 100 000 person-years]; MSSA: 2.7 per 100 000 person-years [95% CI, 2.5-2.9 per 100 000 person-years]) than in women (MRSA: 1.1 per 100 000 person-years [95% CI, 0.9-1.2 per 100 000 person-years]; MSSA: 1.9 per 100 000 person-years [95% CI, 1.7-2.0 per 100 000 person-years]). Rates of bacteremia appeared similar among the 3 TRICARE regions in the continental United States.

For community-onset S aureus SSTIs, rates of both community-onset MRSA (261.2 per 100 000 person-years [95% CI, 257.6-264.8 per 100 000 person-years]) and community-onset MSSA (142.4 per 100 000 person-years [95% CI, 139.8-145.1 per 100 000 person-years]) were highest in those aged 18 to 24 years (Table 5). As with bacteremia, men had higher rates of community-onset MRSA and community-onset MSSA SSTIs than women. However, unlike bacteremia, active duty members had higher rates of community-onset MRSA SSTIs (280.6 per 100 000 person-years [95% CI, 277.1-284.1 per 100 000 person-years]) and community-onset MSSA SSTIs (165.8 per 100 000 person-years [95% CI, 163.1-168.4 per 100 000 person-years]) than nonactive duty individuals (community-onset MRSA SSTIs: 46.0 per 100 000 person-years [95% CI, 45.3-46.6 per 100 000 person-years]; community-onset MSSA SSTIs: 39.4 per 100 000 person-years [95% CI, 38.9-39.9 per 100 000 person-years]). Within the continental United States, the highest rates of community-onset MRSA SSTIs (106.9 per 100 000 person-years [95% CI, 105.4-108.4 per 100 000 person-years]) and community-onset MSSA SSTIs (62.5 per 100 000 person-years [95% CI, 61.4-63.7 per 100 000 person-years]) were seen in the TRICARE region in the South United States. Unadjusted rates of community-onset bacteremia and SSTIs by demographic characteristics for the nonactive duty and active duty subgroups are provided in eTable 4 and eTable 5.

Hospital-Onset S aureus Bacteremia and SSTIs.For hospital-onset S aureus infections, a significant overall trend in the annual rate of infections was seen for hospital-onset MRSA bacteremia (rs = 0.94; P = .005 for trend; Table 3) and hospital-onset MRSA SSTIs (rs = 0.89; P = .02 for trend). In subanalyses of nonactive duty individuals, only hospital-onset MRSA bacteremia decreased significantly from 2005 through 2010 (rs = 0.89; P = .02 for trend; Table 4). The highest rates of hospital-onset S aureus infections were seen in those aged 4 years or younger and 65 years or older (eTable 6). Rates of hospital-onset MRSA and MSSA bacteremia were also higher in men than in women.

Percentage of S aureus Bacteremia and SSTIs That Were MRSA

Fifty-eight percent of community-onset S aureus SSTIs were due to MRSA, significantly higher than for either community-onset bacteremia (39%; P < .001) or hospital-onset SSTIs (53%; P = .02; Figure 1). Fifty-four percent of cases of hospital-onset bacteremia were due to MRSA (P < .001 vs community-onset bacteremia). The proportion of community-onset S aureus SSTIs due to MRSA was 60% in 2005, increased to 62% in 2006, and then decreased each year to a low of 52% in 2010 (P < .001 for trend from 2005-2010; Figure 2). Significant trends were not observed for community-onset bacteremia, hospital-onset bacteremia, or hospital-onset SSTIs (Figure 2). In subanalyses of active duty and nonactive duty individuals, the percentage of community-onset infections due to MRSA was higher in active duty members than nonactive duty beneficiaries (eFigure 1 and eFigure 2), but in both groups the proportion of community-onset SSTIs caused by MRSA decreased significantly from 2005 through 2010 (Figure 3).

Place holder to copy figure label and caption
Figure 1.Staphylococcus aureus Bacteremia and Skin and Soft Tissue Infections (SSTIs) for Overall Population, 2005-2010
Graphic Jump Location

Error bars indicate 95% confidence intervals; MRSA, methicillin-resistant S aureus.
aFor comparison with community-onset SSTIs, the P value was less than .001; for comparison with hospital-onset bacteremia, the P value was less than .001 (both calculated using the χ2 test).
bFor comparison with hospital-onset SSTIs, the P value was .02 (calculated using the χ2 test).
cFor comparison with hospital-onset SSTIs, the P value was .62 (calculated using the χ2 test).

Place holder to copy figure label and caption
Figure 2.Staphylococcus aureus Bacteremia and Skin and Soft Tissue Infections by Onset Setting, 2005-2010
Graphic Jump Location

Error bars indicate 95% confidence intervals; MRSA, methicillin-resistant S aureus. The P values were calculated using Mantel-Haenszel χ2 for linear trend for 2005-2010.

Place holder to copy figure label and caption
Figure 3. Community-Onset Methicillin-Resistant Staphylococcus aureus (MRSA) Skin and Soft Tissue Infection (SSTI) Isolates, 2005-2010
Graphic Jump Location

Error bars represent 95% confidence intervals"P values were calculated using Mantel-Haenszel χ2 for linear trend for 2005-2010.

There are several notable findings from this study examining the epidemiology of S aureus bacteremia and SSTIs. Similar to recent reports by the Centers for Disease Control and Prevention,4,12 the rates of hospital-onset MRSA bacteremia significantly decreased. We found that rates of both community-onset and hospital-onset MRSA bacteremia decreased in parallel. This may be due to an overall decline in health care–associated MRSA bacteremia rather than a decline in true community-associated MRSA bacteremia because we were unable to subclassify community-onset infections as health care–associated community onset. The annual rates of community-onset MSSA bacteremia also decreased significantly. However, the proportions of both community-onset and hospital-onset S aureus bacteremia due to MRSA did not change significantly, suggesting balanced decreases in the rates of both MRSA and MSSA bacteremia.

For community-onset MRSA SSTIs, no significant overall trend in annual rates was observed, but the proportion of community-onset SSTIs due to MRSA declined significantly. While this may represent the replacement of MRSA with MSSA as a cause of community-onset SSTIs, rates of community-onset MSSA SSTIs did not significantly increase during the study. However, the annual rate reductions observed for community-onset MRSA SSTIs after 2008 appeared qualitatively greater than that for community-onset MSSA SSTIs, thereby explaining the increasing percentage of MSSA.

One recent study limited to patients with human immunodeficiency virus in Atlanta, Georgia,17 and 2 preliminary investigations (1 from Chicago, Illinois,18 and 1 from Atlanta19) have also reported that rates of community-onset MRSA SSTIs may have peaked in 2007 or 2008. Therefore, our results for community-onset and hospital-onset S aureus bacteremia and SSTIs in a large geographically diverse population are consistent with the reported changes in hospital-onset MRSA infections from other national investigations,4 provide new data regarding trends in MSSA bacteremia, and are, to our knowledge, the first of a national scope to demonstrate that regional trends in community-onset MRSA SSTIs18,19 may reflect widespread alterations in the epidemiology of community-onset S aureus SSTIs across the United States.

Several epidemiological investigations reporting rates of S aureus bacteremia and SSTIs prior to 2005 described marked increases in the burden of S aureus infections, particularly those due to MRSA. Regional population-based studies of S aureus bacteremia reported stable incidence of S aureus bacteremia overall, but an increasing proportion of cases due to MRSA.9,20 Similarly, Hersh et al21 reported an increase in coded SSTI encounters from 32.1 to 48.1 per 1000 population from 1997 to 2005 coincident with the emergence of community-associated MRSA. Crum et al3 reported an increase in MRSA infections from military facilities in San Diego, California, between 1990 and 2004, with the greatest increase in rates occurring between 2002 and 2004. In an investigation describing community-associated MRSA epidemiology from 2001 through 2002, the annual incidence was 26 per 100 000 person-years, of which 77% of infections were SSTIs.2 This incidence rate is lower than the 46 per 100 000 person-years observed in the current study for SSTIs in nonactive duty beneficiaries, but this may be due to the inability to separate health care–associated community-onset infections from community-associated infections in the current study, as well as different study populations and periods of observation.

The current study also found that the highest rates of community-onset S aureus bacteremia occurred in those at extremes of age (the very young and the elderly), whereas community-onset S aureus SSTI rates were greatest in adults aged 18 through 24 years, men, those serving on active duty, and living in the southern United States. While these observations are in agreement with prior studies,9,10,13,20,22 additional analyses are needed to determine if these characteristics are independent risk factors. The geographic distribution of community-onset SSTI rates may reflect both the influence of climate on SSTIs and the primary locations of military training, where rates of SSTIs are known to be high.23

Previous studies have also used different methods to estimate the national trends in health care–associated S aureus infections, using the International Classification of Diseases, Ninth Revision (ICD-9) codes, to estimate the proportion of infections due to MRSA because there is no MRSA-specific ICD-9 code.22,24 The current study used documented culture results to assess the trends in hospital-onset S aureus bacteremia and SSTIs. While the observed decrease in the annual rates of hospital-onset MRSA bacteremia from the current study is consistent with trends reported by Kallen et al4 and Burton et al,12 the rates in the Department of Defense population were approximately one-tenth of the rates reported by Kallen et al4 (eg, for 2008, 0.5 per 100 000 person-years vs 6.2 per 100 000 person-years, respectively). Unlike the network of large centers from nonrural counties used in the Centers for Disease Control and Prevention report by Kallen et al,4 the Department of Defense health care population is seen at MTFs of varied sizes in urban, semiurban, and rural settings. Additionally, individuals within the TRICARE population seen at MTFs have lower rates of comorbid medical conditions, which are associated with increased S aureus bacteremia risk compared with those seen at an urban tertiary care center, including chronic kidney disease requiring hemodialysis and intravenous drug use.4,20

Most TRICARE beneficiaries also receive open access to care at US MTFs and a reliable income either while on active duty or following retirement. Such factors may mitigate socioeconomic differences that have been associated with increased risk of MRSA infections.13 Findings from other studies have suggested health outcomes within the Department of Defense health care system may be different than other settings.25,26 In addition, the overall age of the current study population may also have reduced rates of S aureus bacteremia because rates of S aureus bacteremia are substantially higher with increasing age.9,20

In addition to the large size and broad geographic distribution represented by the study population, a unique strength of the current study was the ability to evaluate the epidemiology of hospital-onset and community-onset S aureus bacteremia and SSTIs simultaneously. The lines between the hospital and community settings have become less distinct in recent years. Whether the changes in S aureus epidemiology overall were driven by changes within either the hospital or community settings, or both, remains uncertain. Improved infection-control practices may be affecting rates of both hospital-onset and health care–acquired community-onset MRSA bacteremia.4,27

Subsequently, one possibility is that reducing hospital-onset and health care–associated community-onset infections may have an effect on other community-onset S aureus infections. Conversely, studies have shown community-onset MRSA infections, particularly SSTIs, may provide a substantial reservoir of disease, and USA300 strains from the community have become causes of nosocomial infections.10,13 Regardless of the etiology, the concurrent decreases in the rates of hospital-onset and community-onset MRSA bacteremia, coupled with the reduced prevalence of MRSA as a cause of community-onset S aureus SSTIs, are intriguing observations that require further investigation.

Historically large changes in S aureus epidemiology and the strains responsible for disease have occurred.28 For example, phage type 80/81 MRSA strains almost completely disappeared in the 1960s without explanation after causing widespread disease in the 1950s.28 Recent investigations have reported longitudinal changes in the strains responsible for nosocomial or invasive MRSA infections,2931 but similar data for SSTIs or infections due to MSSA since 2008 are lacking.

There are limitations to this observational study. First, data prior to January 1, 2005, were not available for analysis to evaluate trends in S aureus bacteremia or SSTIs since the emergence of community-acquired MRSA. Second, clinical information allowing classification of SSTIs as surgical site infections, cutaneous abscesses, or cellulitis was not available. Wound or abscess culture results were also not categorized by tissue site, although skin and skin structure–related infections are the most common manifestation of community-onset MRSA disease.13 Third, data regarding self-reported race and ethnicity, and clinical outcomes, including mortality, also were not available. Fourth, due to constraints of the available data, it was not possible to perform modeling of the rates at the person level, adjusting for covariables or sensitivity analyses. Fifth, some TRICARE beneficiaries (predominantly retirees and their dependents) may obtain care at nonmilitary facilities. Subsequently, the rates of S aureus bacteremia and SSTIs we observed likely underestimate the true burden of disease within this patient population. However, while changing access to care and referral patterns would bias infection rates, systematic TRICARE referral and access to care policies did not change during the course of this study.32 Similarly, a reduction in the number of overall cultures obtained may have affected the observed rates of S aureus bacteremia and SSTIs. However, the decreasing proportions of all cultures positive for S aureus, including MRSA, provide further support that the trends observed for the rates of S aureus bacteremia and SSTIs reflect true decreases in the burden of S aureus disease, particularly MRSA. Additionally, the relatively stable size of the study population and the large number of isolates should minimize the effect of differences in local practice patterns regarding culturing on the conclusions of the current study.

The study population also has some unique characteristics. Active duty military members are young, healthy, have open access to care, and have increased risk of SSTIs due to military training and other job-related exposures. Active duty members had substantially higher rates of SSTIs, and a higher proportion of both bacteremia and SSTIs due to MRSA than nonactive duty individuals. However, nonactive duty beneficiaries comprised approximately 85% of the study population, and subanalyses revealed that even though the annual rates of bacteremia and SSTIs were different for active duty compared with nonactive duty beneficiaries, the significant trends for bacteremia and SSTIs observed for both these subpopulations were in agreement. While the overall rates of disease were likely influenced by the characteristics of the Department of Defense population, the observed trends were consistent with investigations in other US populations.4,12

In conclusion, within the US Military Health System, which provides care to both nonactive duty and active duty beneficiaries, the burden of S aureus bacteremia and SSTIs remains substantial, highlighting the importance of having successful prevention and treatment strategies. The rates of community-onset MRSA and MSSA bacteremia and hospital-onset MRSA bacteremia decreased from 2005 through 2010, as the proportion of community-onset SSTIs due to MRSA decreased. These observations, taken together with results from others showing decreases in the rates of health care–associated infections from MRSA,4 suggest that broad shifts in the epidemiology of S aureus infections may be occurring. Additional studies are needed to assess whether these trends will continue, which prevention methods are most effective, and to what degree other factors may be contributing.

Corresponding Author: Clinton K. Murray, MD, San Antonio Military Medical Center, 3551 Roger Brooke Dr, Infectious Disease Service, Fort Sam Houston, TX 78234 (clinton.murray@amedd.army.mil).

Author Contributions: Drs Landrum and Murray had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Landrum, Chukwuma, Murray.

Acquisition of data: Neumann, Cook, Chukwuma.

Analysis and interpretation of data: Landrum, Neumann, Cook, Chukwuma, Ellis, Hospenthal, Murray.

Drafting of the manuscript: Landrum, Chukwuma, Murray.

Critical revision of the manuscript for important intellectual content: Neumann, Cook, Chukwuma, Ellis, Hospenthal, Murray.

Statistical analysis: Landrum, Neumann, Cook, Chukwuma.

Administrative, technical, or material support: Chukwuma, Murray.

Study supervision: Landrum, Murray.

Conflict of Interest Disclosures: The authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.

Funding/Support: This project has been funded in part with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, under interagency agreement Y1-AI-5072. Support for this work was leveraged from grants provided by the Global Emerging Infections Surveillance and Response Program, Armed Forces Health Surveillance Center to the EpiData Center Department, Navy and Marine Corps Public Health Center (NMCPHC). Additional support was also provided in part by an appointment to the Postgraduate Research Participation Program at the Navy and Marine Corps Public Health Center administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the US Department of Energy and the NMCPHC. At the time of the research for this study and writing of this article, Dr Landrum was an employee of the Infectious Disease Clinical Research Program (IDCRP). As such, he received support for this work provided by the IDCRP, a Department of Defense program executed through the Uniformed Services University of the Health Sciences.

Role of the Sponsors: The NMCPHC and IDCRP reviewed and approved the manuscript, but had no role in design and conduct of the study; collection, management, analysis, and interpretation of the data; or in the preparation of the manuscript.

Disclaimer: Some of the authors of this article are military service members and/or employees of the US government. As such, this work was prepared as part of official duties. Title 17 USC 105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 USC 101 defines a United States Government work as “a work prepared by a military service member or employee of the United States Government as part of that person's official duties.” The content of this publication is the sole responsibility of the authors and does not necessarily reflect the views or policies of the National Institutes of Health or the Department of Health and Human Services, the Department of Defense, or the departments of the Army, Navy, or Air Force. Mention of trade names, commercial products, or organizations does not imply endorsement by the US government.

Previous Presentation: These data were presented in part at the 49th Annual Meeting of the Infectious Diseases Society of America; October 19-23, 2011; Boston, Massachusetts.

Online-Only Material: The Author Video Interview is available .

Herold BC, Immergluck LC, Maranan MC,  et al.  Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk.  JAMA. 1998;279(8):593-598
PubMed   |  Link to Article
Fridkin SK, Hageman JC, Morrison M,  et al; Active Bacterial Core Surveillance Program of the Emerging Infections Program Network.  Methicillin-resistant Staphylococcus aureus disease in three communities.  N Engl J Med. 2005;352(14):1436-1444
PubMed   |  Link to Article
Crum NF, Lee RU, Thornton SA,  et al.  Fifteen-year study of the changing epidemiology of methicillin-resistant Staphylococcus aureus.  Am J Med. 2006;119(11):943-951
PubMed   |  Link to Article
Kallen AJ, Mu Y, Bulens S,  et al; Active Bacterial Core surveillance (ABCs) MRSA Investigators of the Emerging Infections Program.  Health care-associated invasive MRSA infections, 2005-2008.  JAMA. 2010;304(6):641-648
PubMed   |  Link to Article
Centers for Disease Control and Prevention (CDC).  Methicillin-resistant Staphylococcus aureus infections in correctional facilities---Georgia, California, and Texas, 2001-2003.  MMWR Morb Mortal Wkly Rep. 2003;52(41):992-996
PubMed
Kazakova SV, Hageman JC, Matava M,  et al.  A clone of methicillin-resistant Staphylococcus aureus among professional football players.  N Engl J Med. 2005;352(5):468-475
PubMed   |  Link to Article
Ellis MW, Griffith ME, Dooley DP,  et al.  Targeted intranasal mupirocin to prevent colonization and infection by community-associated methicillin-resistant Staphylococcus aureus strains in soldiers: a cluster randomized controlled trial.  Antimicrob Agents Chemother. 2007;51(10):3591-3598
PubMed   |  Link to Article
Whitman TJ, Herlihy RK, Schlett CD,  et al.  Chlorhexidine-impregnated cloths to prevent skin and soft-tissue infection in Marine recruits: a cluster-randomized, double-blind, controlled effectiveness trial.  Infect Control Hosp Epidemiol. 2010;31(12):1207-1215
PubMed   |  Link to Article
El Atrouni WI, Knoll BM, Lahr BD, Eckel-Passow JE, Sia IG, Baddour LM. Temporal trends in the incidence of Staphylococcus aureus bacteremia in Olmsted County, Minnesota, 1998 to 2005: a population-based study.  Clin Infect Dis. 2009;49(12):e130-e138
PubMed   |  Link to Article
Klevens RM, Morrison MA, Nadle J,  et al; Active Bacterial Core surveillance (ABCs) MRSA Investigators.  Invasive methicillin-resistant Staphylococcus aureus infections in the United States.  JAMA. 2007;298(15):1763-1771
PubMed   |  Link to Article
Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R.National Nosocomial Infections Surveillance System.  Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992-2003.  Clin Infect Dis. 2006;42(3):389-391
PubMed   |  Link to Article
Burton DC, Edwards JR, Horan TC, Jernigan JA, Fridkin SK. Methicillin-resistant Staphylococcus aureus central line-associated bloodstream infections in US intensive care units, 1997-2007.  JAMA. 2009;301(7):727-736
PubMed   |  Link to Article
Liu C, Graber CJ, Karr M,  et al.  A population-based study of the incidence and molecular epidemiology of methicillin-resistant Staphylococcus aureus disease in San Francisco, 2004-2005.  Clin Infect Dis. 2008;46(11):1637-1646
PubMed   |  Link to Article
Velasco D, del Mar Tomas M, Cartelle M,  et al.  Evaluation of different methods for detecting methicillin (oxacillin) resistance in Staphylococcus aureus.  J Antimicrob Chemother. 2005;55(3):379-382
PubMed   |  Link to Article
Cohen AL, Calfee D, Fridkin SK,  et al; Society for Healthcare Epidemiology of America and the Healthcare Infection Control Practices Advisory Committee.  Recommendations for metrics for multidrug-resistant organisms in healthcare settings: SHEA/HICPAC Position paper.  Infect Control Hosp Epidemiol. 2008;29(10):901-913
PubMed   |  Link to Article
Roalfe AK, Holder RL, Wilson S. Standardisation of rates using logistic regression: a comparison with the direct method.  BMC Health Serv Res. 2008;8:275
PubMed   |  Link to Article
Hidron AI, Moanna A, Rimland D. The rise and fall of methicillin-resistant Staphylococcus aureus infections in HIV patients.  AIDS. 2011;25(7):1001-1003
PubMed   |  Link to Article
Popovich KJ, David MZ, Grasso AE, Daum RS, Hota B, Lauderdale DS. Community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) skin and soft tissue infections (SSTI) in Chicago, 2005-8: high-risk clusters and trends in incidence. Paper presented at: 49th Annual Meeting of the Infectious Diseases Society of America; October 20-23, 2011; Boston, MA
Stenehjem E, Stafford C, Rimland D. Reduction in MRSA infections among veterans. Paper presented at: 49th Annual Meeting of the Infectious Diseases Society of America; October 20-23, 2011; Boston, MA
Laupland KB, Ross T, Gregson DB. Staphylococcus aureus bloodstream infections: risk factors, outcomes, and the influence of methicillin resistance in Calgary, Canada, 2000-2006.  J Infect Dis. 2008;198(3):336-343
PubMed   |  Link to Article
Hersh AL, Chambers HF, Maselli JH, Gonzales R. National trends in ambulatory visits and antibiotic prescribing for skin and soft-tissue infections.  Arch Intern Med. 2008;168(14):1585-1591
PubMed   |  Link to Article
Kuehnert MJ, Hill HA, Kupronis BA, Tokars JI, Solomon SL, Jernigan DB. Methicillin-resistant- Staphylococcus aureus hospitalizations, United States.  Emerg Infect Dis. 2005;11(6):868-872
PubMed   |  Link to Article
Army Medical Surveillance Activity.  Cellulitis and abscess, active components, US Armed Forces, 2002-2005.  Med Surveillance Monthly Rep. 2006;12(4):208
Klein E, Smith DL, Laxminarayan R. Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005.  Emerg Infect Dis. 2007;13(12):1840-1846
PubMed   |  Link to Article
Halsell JS, Riddle JR, Atwood JE,  et al; Department of Defense Smallpox Vaccination Clinical Evaluation Team.  Myopericarditis following smallpox vaccination among vaccinia-naive US military personnel.  JAMA. 2003;289(24):3283-3289
PubMed   |  Link to Article
Marconi VC, Grandits GA, Weintrob AC,  et al; Infectious Disease Clinical Research Program HIV Working Group (IDCRP).  Outcomes of highly active antiretroviral therapy in the context of universal access to healthcare: the US Military HIV Natural History Study.  AIDS Res Ther. 2010;7:14
PubMed   |  Link to Article
Jain R, Kralovic SM, Evans ME,  et al.  Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections.  N Engl J Med. 2011;364(15):1419-1430
PubMed   |  Link to Article
Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era.  Nat Rev Microbiol. 2009;7(9):629-641
PubMed   |  Link to Article
Kern WV. Management of Staphylococcus aureus bacteremia and endocarditis: progresses and challenges.  Curr Opin Infect Dis. 2010;23(4):346-358
PubMed   |  Link to Article
Jenkins TC, McCollister BD, Sharma R,  et al.  Epidemiology of healthcare-associated bloodstream infection caused by USA300 strains of methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals.  Infect Control Hosp Epidemiol. 2009;30(3):233-241
PubMed   |  Link to Article
Seybold U, Kourbatova EV, Johnson JG,  et al.  Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections.  Clin Infect Dis. 2006;42(5):647-656
PubMed   |  Link to Article
US Department of Defense.  TRICARE policy for access to care, HA policy 11-005. http://www.health.mil/libraries/HA_Policies_and_Guidelines/11-005.pdf. Accessed September 19, 2011

Figures

Place holder to copy figure label and caption
Figure 1.Staphylococcus aureus Bacteremia and Skin and Soft Tissue Infections (SSTIs) for Overall Population, 2005-2010
Graphic Jump Location

Error bars indicate 95% confidence intervals; MRSA, methicillin-resistant S aureus.
aFor comparison with community-onset SSTIs, the P value was less than .001; for comparison with hospital-onset bacteremia, the P value was less than .001 (both calculated using the χ2 test).
bFor comparison with hospital-onset SSTIs, the P value was .02 (calculated using the χ2 test).
cFor comparison with hospital-onset SSTIs, the P value was .62 (calculated using the χ2 test).

Place holder to copy figure label and caption
Figure 2.Staphylococcus aureus Bacteremia and Skin and Soft Tissue Infections by Onset Setting, 2005-2010
Graphic Jump Location

Error bars indicate 95% confidence intervals; MRSA, methicillin-resistant S aureus. The P values were calculated using Mantel-Haenszel χ2 for linear trend for 2005-2010.

Place holder to copy figure label and caption
Figure 3. Community-Onset Methicillin-Resistant Staphylococcus aureus (MRSA) Skin and Soft Tissue Infection (SSTI) Isolates, 2005-2010
Graphic Jump Location

Error bars represent 95% confidence intervals"P values were calculated using Mantel-Haenszel χ2 for linear trend for 2005-2010.

Tables

Table Graphic Jump LocationTable 1. Demographic Characteristics of US Department of Defense TRICARE Beneficiaries, 2005-2010
Table Graphic Jump LocationTable 2. Positive Blood and Wound Abscess Cultures in TRICARE Beneficiaries
Table Graphic Jump LocationTable 3.Staphylococcus aureus Infections by Setting, Culture Type, and Methicillin Resistance for Overall Study Population
Table Graphic Jump LocationTable 4.Staphylococcus aureus Infections by Setting, Culture Type, and Methicillin Resistance for Nonactive Duty Study Subpopulation
Table Graphic Jump LocationTable 5. Community-Onset Staphylococcus aureus Infections for Overall Study Population

References

Herold BC, Immergluck LC, Maranan MC,  et al.  Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk.  JAMA. 1998;279(8):593-598
PubMed   |  Link to Article
Fridkin SK, Hageman JC, Morrison M,  et al; Active Bacterial Core Surveillance Program of the Emerging Infections Program Network.  Methicillin-resistant Staphylococcus aureus disease in three communities.  N Engl J Med. 2005;352(14):1436-1444
PubMed   |  Link to Article
Crum NF, Lee RU, Thornton SA,  et al.  Fifteen-year study of the changing epidemiology of methicillin-resistant Staphylococcus aureus.  Am J Med. 2006;119(11):943-951
PubMed   |  Link to Article
Kallen AJ, Mu Y, Bulens S,  et al; Active Bacterial Core surveillance (ABCs) MRSA Investigators of the Emerging Infections Program.  Health care-associated invasive MRSA infections, 2005-2008.  JAMA. 2010;304(6):641-648
PubMed   |  Link to Article
Centers for Disease Control and Prevention (CDC).  Methicillin-resistant Staphylococcus aureus infections in correctional facilities---Georgia, California, and Texas, 2001-2003.  MMWR Morb Mortal Wkly Rep. 2003;52(41):992-996
PubMed
Kazakova SV, Hageman JC, Matava M,  et al.  A clone of methicillin-resistant Staphylococcus aureus among professional football players.  N Engl J Med. 2005;352(5):468-475
PubMed   |  Link to Article
Ellis MW, Griffith ME, Dooley DP,  et al.  Targeted intranasal mupirocin to prevent colonization and infection by community-associated methicillin-resistant Staphylococcus aureus strains in soldiers: a cluster randomized controlled trial.  Antimicrob Agents Chemother. 2007;51(10):3591-3598
PubMed   |  Link to Article
Whitman TJ, Herlihy RK, Schlett CD,  et al.  Chlorhexidine-impregnated cloths to prevent skin and soft-tissue infection in Marine recruits: a cluster-randomized, double-blind, controlled effectiveness trial.  Infect Control Hosp Epidemiol. 2010;31(12):1207-1215
PubMed   |  Link to Article
El Atrouni WI, Knoll BM, Lahr BD, Eckel-Passow JE, Sia IG, Baddour LM. Temporal trends in the incidence of Staphylococcus aureus bacteremia in Olmsted County, Minnesota, 1998 to 2005: a population-based study.  Clin Infect Dis. 2009;49(12):e130-e138
PubMed   |  Link to Article
Klevens RM, Morrison MA, Nadle J,  et al; Active Bacterial Core surveillance (ABCs) MRSA Investigators.  Invasive methicillin-resistant Staphylococcus aureus infections in the United States.  JAMA. 2007;298(15):1763-1771
PubMed   |  Link to Article
Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R.National Nosocomial Infections Surveillance System.  Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992-2003.  Clin Infect Dis. 2006;42(3):389-391
PubMed   |  Link to Article
Burton DC, Edwards JR, Horan TC, Jernigan JA, Fridkin SK. Methicillin-resistant Staphylococcus aureus central line-associated bloodstream infections in US intensive care units, 1997-2007.  JAMA. 2009;301(7):727-736
PubMed   |  Link to Article
Liu C, Graber CJ, Karr M,  et al.  A population-based study of the incidence and molecular epidemiology of methicillin-resistant Staphylococcus aureus disease in San Francisco, 2004-2005.  Clin Infect Dis. 2008;46(11):1637-1646
PubMed   |  Link to Article
Velasco D, del Mar Tomas M, Cartelle M,  et al.  Evaluation of different methods for detecting methicillin (oxacillin) resistance in Staphylococcus aureus.  J Antimicrob Chemother. 2005;55(3):379-382
PubMed   |  Link to Article
Cohen AL, Calfee D, Fridkin SK,  et al; Society for Healthcare Epidemiology of America and the Healthcare Infection Control Practices Advisory Committee.  Recommendations for metrics for multidrug-resistant organisms in healthcare settings: SHEA/HICPAC Position paper.  Infect Control Hosp Epidemiol. 2008;29(10):901-913
PubMed   |  Link to Article
Roalfe AK, Holder RL, Wilson S. Standardisation of rates using logistic regression: a comparison with the direct method.  BMC Health Serv Res. 2008;8:275
PubMed   |  Link to Article
Hidron AI, Moanna A, Rimland D. The rise and fall of methicillin-resistant Staphylococcus aureus infections in HIV patients.  AIDS. 2011;25(7):1001-1003
PubMed   |  Link to Article
Popovich KJ, David MZ, Grasso AE, Daum RS, Hota B, Lauderdale DS. Community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) skin and soft tissue infections (SSTI) in Chicago, 2005-8: high-risk clusters and trends in incidence. Paper presented at: 49th Annual Meeting of the Infectious Diseases Society of America; October 20-23, 2011; Boston, MA
Stenehjem E, Stafford C, Rimland D. Reduction in MRSA infections among veterans. Paper presented at: 49th Annual Meeting of the Infectious Diseases Society of America; October 20-23, 2011; Boston, MA
Laupland KB, Ross T, Gregson DB. Staphylococcus aureus bloodstream infections: risk factors, outcomes, and the influence of methicillin resistance in Calgary, Canada, 2000-2006.  J Infect Dis. 2008;198(3):336-343
PubMed   |  Link to Article
Hersh AL, Chambers HF, Maselli JH, Gonzales R. National trends in ambulatory visits and antibiotic prescribing for skin and soft-tissue infections.  Arch Intern Med. 2008;168(14):1585-1591
PubMed   |  Link to Article
Kuehnert MJ, Hill HA, Kupronis BA, Tokars JI, Solomon SL, Jernigan DB. Methicillin-resistant- Staphylococcus aureus hospitalizations, United States.  Emerg Infect Dis. 2005;11(6):868-872
PubMed   |  Link to Article
Army Medical Surveillance Activity.  Cellulitis and abscess, active components, US Armed Forces, 2002-2005.  Med Surveillance Monthly Rep. 2006;12(4):208
Klein E, Smith DL, Laxminarayan R. Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005.  Emerg Infect Dis. 2007;13(12):1840-1846
PubMed   |  Link to Article
Halsell JS, Riddle JR, Atwood JE,  et al; Department of Defense Smallpox Vaccination Clinical Evaluation Team.  Myopericarditis following smallpox vaccination among vaccinia-naive US military personnel.  JAMA. 2003;289(24):3283-3289
PubMed   |  Link to Article
Marconi VC, Grandits GA, Weintrob AC,  et al; Infectious Disease Clinical Research Program HIV Working Group (IDCRP).  Outcomes of highly active antiretroviral therapy in the context of universal access to healthcare: the US Military HIV Natural History Study.  AIDS Res Ther. 2010;7:14
PubMed   |  Link to Article
Jain R, Kralovic SM, Evans ME,  et al.  Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections.  N Engl J Med. 2011;364(15):1419-1430
PubMed   |  Link to Article
Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era.  Nat Rev Microbiol. 2009;7(9):629-641
PubMed   |  Link to Article
Kern WV. Management of Staphylococcus aureus bacteremia and endocarditis: progresses and challenges.  Curr Opin Infect Dis. 2010;23(4):346-358
PubMed   |  Link to Article
Jenkins TC, McCollister BD, Sharma R,  et al.  Epidemiology of healthcare-associated bloodstream infection caused by USA300 strains of methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals.  Infect Control Hosp Epidemiol. 2009;30(3):233-241
PubMed   |  Link to Article
Seybold U, Kourbatova EV, Johnson JG,  et al.  Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections.  Clin Infect Dis. 2006;42(5):647-656
PubMed   |  Link to Article
US Department of Defense.  TRICARE policy for access to care, HA policy 11-005. http://www.health.mil/libraries/HA_Policies_and_Guidelines/11-005.pdf. Accessed September 19, 2011
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