Abstract

Background

Studies have shown that healthcare-associated infections (HAIs) due to methicillin-resistant Staphylococcus aureus (MRSA) can lead to substantial healthcare costs in acute care settings. However, little is known regarding the consequences of these infections on patients in long-term care centers (LTCCs). The purpose of this study was to estimate the attributable cost of MRSA HAIs in LTCCs within the Department of Veterans Affairs (VA).

Methods

We performed a retrospective cohort study of patients admitted to VA LTCCs between 1 January 2009 and 30 September 2015. MRSA HAIs were defined as a positive clinical culture at least 48 hours after LTCC admission so as to exclude community-acquired infections. Positive cultures were further classified by site (sterile or nonsterile). We used multivariable generalized linear models and 2-part models to compare the LTCC and acute care costs between patients with and without an MRSA HAI.

Results

In our primary analysis, there was no difference in LTCC costs between patients with and without a MRSA HAI. There was, however, a significant increase in the odds of being transferred to an acute care facility (odds ratio, 4.40 [95% confidence interval {CI}, 3.40–5.67]) and in acute care costs ($9711 [95% CI, $6961–$12 462]).

Conclusions

Our findings of high cost and increased risk of transfer from LTCC to acute care are important because they highlight the substantial clinical and economic impact of MRSA infections in this population.

Because patients in long-term care centers (LTCCs) often have numerous chronic diseases, in-dwelling devices such as feeding tubes or urinary catheters, and long histories of exposure to a variety of healthcare settings, they are at high risk for colonization and infection with multidrug-resistant organisms (MDROs) [1, 2]. Colonization with these organisms has been found to be more common in LTCCs than in acute care facilities [3]. More than one-third of LTCC residents are colonized with an MDRO [3–6], and acquisition is quite common among this population [5].

In January 2009, the United States (US) Department of Veterans Affairs (VA) implemented a methicillin-resistant Staphylococcus aureus (MRSA) prevention initiative in its 133 LTCCs. Similar to the initiative implemented in VA acute care facilities in October 2007, it consisted of a bundle of strategies including nasal surveillance for MRSA, contact precautions for patients who test positive for MRSA, improved hand hygiene, and institutional culture change to emphasize that all healthcare providers are responsible for infection prevention and control [7]. In 2013, infection prevention in LTCCs was declared a national priority by the US Department of Health and Human Services [8]. In addition, a number of professional organizations have issued guidelines for infection control practices in LTCC settings [7, 9].

Economic evaluations—such as cost-effectiveness analyses—of infection control interventions are essential tools that can help decision makers better understand how to make best use of scarce resources to improve patient safety outcomes. Often, these evaluations are conducted using simulation models that include parameters such as the cost of the intervention, the impact of the intervention on infection rates, and the attributable cost of infections that would be prevented. While a number of estimates of the attributable cost of MRSA healthcare-associated infections (HAIs) among patients in acute care settings have been published [10, 11], none have been published for HAIs among LTCC patients. A primary driver of the attributable cost of HAIs identified in the acute care setting is the additional days that a patient needs to spend in the hospital. However, this would likely not be the case for LTCC patients since the patient would be staying in the facility for an extended period of time regardless of whether an infection was present. These estimates could be used as input parameters for an economic evaluation of MRSA prevention interventions or programs but are also useful in quantifying the opportunity cost of resources utilized to care for these patients, which could be used for other purposes. Therefore, it is useful to estimate the attributable cost of infections in specific settings rather than simply using previously generated estimates from the acute care setting. To fill this gap in the literature, our goal in this study was to estimate the attributable cost of MRSA HAIs among LTCC patients in the VA system.

METHODS

Setting

As the largest integrated healthcare system in the US, the VA provides care for a unique patient population: individuals who served in active duty in one of the armed forces. Of the roughly 22 million Veterans in the US, nearly 9 million are enrolled in the VA [12], and approximately 6 million Veterans per year [13] receive care in one of 150 VA acute care faculties, >100 LTCC facilities, or >1000 outpatient clinics in the US [14]. The VA electronic medical record (EMR), which includes data from both VA acute care and LTCC facilities, was one of the first such systems in the US [15].

Data

The VA EMR contains the results from microbiology tests as free text. To convert this unstructured information into a structured format that would allow it to be used in a statistical analysis, our team developed a natural language processing tool to extract information regarding organism, antibiotic susceptibility, and specimen location [16]. These data were used to identify which LTCC patients from our cohort developed MRSA HAIs, when these HAIs were identified, and the body site from which the clinical culture was obtained.

Healthcare cost data were obtained from the VA Managerial Cost Accounting (MCA) System [17], which is an activity-based accounting system. Physicians and managers report their activities, which are then used to distribute costs from the VA payroll and general ledger [18]. These personnel costs are combined with the costs of intermediate goods—such as radiographs, units of blood, or days in the intensive care unit (ICU)—to generate the costs of institutional (whether in an LTCC or an acute care facility) stays and outpatient encounters. Cost data for institutional stays, such as LTCCs or acute care facilities, are available from the MCA system for each calendar month of a patient’s stay [18]. In other words, if a patient is admitted during one month (eg, 25 October) and discharged during the following month (eg, 5 November), then the system would generate separate records for those services used and costs incurred during the first month (eg, from 25 to 31 October) and those used and incurred during the second month (eg, 1–5 November). This dataset also contains separate records for each “treating specialty” or ward location during an institutional stay, allowing us to separate costs in a LTCC setting from those in an acute care setting for patients who were transferred from the LTCC facility to an acute care facility for a period of time. As will be described in more detail below, we used this characteristic of the data to more accurately estimate the attributable cost of MRSA HAIs among patients admitted to LTCC facilities.

Patient demographic and clinical characteristics were obtained from the VA Corporate Data Warehouse, a national repository for electronic data from several different administrative and clinical data sources in the VA.

Study Design and Population

We used a historical cohort design with patients admitted to a VA LTCC between 1 January 2009 and 30 September 2015.

We conducted our primary analysis so as to minimize the effects of time-dependent bias. This bias can arise when an exposure, such as an HAI, can occur at any time during the LTCC episode, yet costs are compared for the complete LTCC episode. Because time-dependent bias can lead to overestimation of the effects of HAIs on patient outcomes [19], efforts to reduce this bias can lead to more accurate results. One strategy for reducing this bias is to shift the index date from the LTCC admission date to the exposure date and analyzing only outcomes over the postexposure time period [20]. We employed this approach for addressing time-dependent bias by exploiting the structure of the MCA inpatient cost data structure in which costs can be separated by calendar month. In our analysis, we limited the MRSA HAIs to only those occurring on the first day of a calendar month starting with the second calendar month. We excluded MRSA HAIs that occurred during the first calendar month because a full month of cost following the event would not be available. Because LTCC stays may last many months or even years, we included MRSA HAIs that occurred on the first day of the third month, fourth month, and so on. For each patient with an MRSA HAI cultured on the first day of a calendar month of their LTCC stay, we randomly selected up to 10 control patients from the same LTCC who had the same admitting diagnosis but had not had a positive culture up until that point in their LTCC stay using an exposure density sampling approach [21]. We repeated this process for each month until month 13 and pooled the resultant matched patients for our analysis. The index date was the MRSA HAI date for patients included in the analysis with an infection and the first day of the calendar month for which a match occurred for patients without an infection. In addition, we conducted secondary analyses in which we expanded our definition of MRSA HAI to include the first day of the calendar month ± 1 day and ± 2 days. We have employed a similar strategy to reduce time-dependent bias in estimating the cost of HAIs in the acute care setting [10, 11].

Outcome Variables

VA MCA data allow inpatient costs to be separated into fixed and variable costs, a distinction that is important in the estimation of costs attributable to MRSA HAIs [22]. Fixed costs are those that are associated with long-term obligations and are difficult to change in the short run. Examples of fixed costs in healthcare include contractual commitments such as staff employment or lease agreements on diagnostic devices and physical commitments such as investments in buildings and infrastructure. Variable costs, such as drugs and consumables, can be avoided in the short run and therefore represent expenditures that could be saved if an HAI is prevented. We report results for both total and variable inpatient costs. In our primary analysis, costs were captured during the month following index date under the assumption that most of the increases in cost following MRSA HAIs would occur during this time period. In addition, we relaxed this assumption and captured costs from the index date until the end of the Veteran’s stay in the LTCC. Finally, because patients admitted to a LTCC could be transferred to an acute care facility if more intensive medical care was necessary [23–25], we categorized patient location as being LTCC or acute care and estimated the impact of MRSA HAI on the cost for each setting separately.

Independent Variables

The key independent variable in our analyses was an MRSA HAI, defined as a positive culture obtained after the first 2 days of a patient’s LTCC admission. Positive cultures in administrative datasets may be evidence of a true infection, or they may indicate colonization. We classified positive cultures based on whether they were obtained from a body site that is typically sterile. Those from sterile sites (blood, cerebrospinal fluid, pleural fluid, and synovial fluid) were deemed invasive infections while all other cultures were considered noninvasive.

Other independent variables in our analyses included demographic characteristics (age, race, marital status, insurance status, sex); healthcare costs in the 365 days prior to admission; cost in the LTCC prior to index date; and comorbidities as measured using a risk index that combines the Charlson and Elixhauser indices [26]. This comorbidity index is created by assigning weights to specific conditions ranging from –1 for human immunodeficiency virus/AIDS and hypertension to 5 for metastatic cancer. In our population, the values for this index ranged from –2 to 17 with higher values associated with increased risk of mortality.

Statistical Analyses

We performed multivariable cost regressions on our pooled cohort of matched patients from each calendar month. Because the match process may have selected the same patient more than once (for example, a patient selected as a control for one month could, in a subsequent month, be randomly selected as a control or develop an infection) we clustered the standard errors for these regression models at the individual level. As in similar analyses for HAIs identified in acute care settings conducted previously, we used a generalized linear model with a gamma “family” and log link function for LTCC costs [10, 11]. Because not all patients would necessarily be transferred to an acute care facility, we used a 2-part model to assess acute care costs. In the first part of this 2-part model, we employed a logistic model with a binary dependent variable for whether the patient had any acute care cost. In the second part, we used a generalized linear model with a gamma family and log link function for those patients with positive acute care cost. In addition to our primary analysis of 1-month costs among patients whose exposure occurred on the first day of a calendar month, secondary analyses included extending the follow-up period through discharge from the LTCC and expanding our definition of MRSA HAI to include the first day of the calendar month ± 1 day and ± 2 days.

RESULTS

Of the 2982 patients both with and without an MRSA who were included in our primary analysis, 307 had a qualifying MRSA HAI that began on the first day of the second or a later calendar month. In general, those with and without MRSA HAIs were similar in terms of age, race, and insurance coverage (Table 1). Those with MRSA HAIs, however, did have slightly higher comorbidity index values (4.4 vs 4.0), LTCC costs in the 365-day period prior to index date ($70 250 vs $64 837), and inpatient acute care costs in the 365-day period prior to admission ($100 078 vs $82 953).

Table 1.

Descriptive Statistics for Patient Characteristics: Methicillin-Resistant Staphylococcus aureus Healthcare-Associated Infection on First Day of Calendar Month

CharacteristicsNo MRSA HAIMRSA HAI
No.(%)No.(%)
Total No.2675307
Age, mean (SD)71.2(12.3)71.3(11.9)
Female sex71(2.65%)6(1.95%)
Race/ethnicity
 White2049(76.60%)226(73.62%)
 Black457(17.08%)56(18.24%)
 Other/unknown/missing169(6.32%)25(8.14%)
Marital status
 Married878(32.82%)105(34.20%)
 Never married40(1.50%)(0.00%)
 Divorced846(31.63%)103(33.55%)
 Separated99(3.70%)3(0.98%)
 Widowed394(14.73%)50(16.29%)
 Unknown/missing52(1.94%)6(1.95%)
VA priority groupa
 11079(40.34%)129(42.02%)
 2186(6.95%)34(11.07%)
 3388(14.50%)40(13.03%)
 4151(5.64%)20(6.51%)
 5–6870(32.52%)84(27.36%)
Insurance
 No insurance2275(85.05%)269(87.62%)
 Insurance299(11.18%)26(8.47%)
 Missing101(3.78%)12(3.91%)
VRE infection in 365 d prior to admission104(3.89%)15(4.89%)
Comorbidity index, mean 4.03.24.43.2
Total LTCC cost prior to index date$64 837 $71 894 $70 250 $84 340
Inpatient cost in 365 d prior to admission$82 953 $152 548 $100 078 $201 254
Outpatient cost in 365 d prior to admission$17 642 $21 361 $18 541 $20 374
CharacteristicsNo MRSA HAIMRSA HAI
No.(%)No.(%)
Total No.2675307
Age, mean (SD)71.2(12.3)71.3(11.9)
Female sex71(2.65%)6(1.95%)
Race/ethnicity
 White2049(76.60%)226(73.62%)
 Black457(17.08%)56(18.24%)
 Other/unknown/missing169(6.32%)25(8.14%)
Marital status
 Married878(32.82%)105(34.20%)
 Never married40(1.50%)(0.00%)
 Divorced846(31.63%)103(33.55%)
 Separated99(3.70%)3(0.98%)
 Widowed394(14.73%)50(16.29%)
 Unknown/missing52(1.94%)6(1.95%)
VA priority groupa
 11079(40.34%)129(42.02%)
 2186(6.95%)34(11.07%)
 3388(14.50%)40(13.03%)
 4151(5.64%)20(6.51%)
 5–6870(32.52%)84(27.36%)
Insurance
 No insurance2275(85.05%)269(87.62%)
 Insurance299(11.18%)26(8.47%)
 Missing101(3.78%)12(3.91%)
VRE infection in 365 d prior to admission104(3.89%)15(4.89%)
Comorbidity index, mean 4.03.24.43.2
Total LTCC cost prior to index date$64 837 $71 894 $70 250 $84 340
Inpatient cost in 365 d prior to admission$82 953 $152 548 $100 078 $201 254
Outpatient cost in 365 d prior to admission$17 642 $21 361 $18 541 $20 374

Data are presented as No. (%) unless otherwise indicated.

Abbreviations: HAI, healthcare-associated infection; LTCC, long-term care center; MRSA, methicillin-resistant Staphylococcus aureus; SD, standard deviation; VA, Veterans Affairs; VRE, vancomycin-resistant enterococci.

aVA enrollment priority groups are defined as follows:

Priority Group 1: Veterans with service-connected disabilities 50% or more disabling or whose service-connected conditions cause them to be unemployable.

Priority Group 2: Veterans with service-connected disabilities 30%–40% disabling.

Priority Group 3: Veterans who are former prisoners of war, were awarded a Purple Heart medal, were discharged from the military due to a disability incurred or aggravated in the line of duty, with service-connected disability 10%–20% disabling, were disabled by treatment or vocational rehabilitation, or were awarded the Medal of Honor.

Priority Group 4: Veterans who are receiving aid or household benefits from VA or who are catastrophically disabled.

Priority Group 5: Nonservice-connected veterans and service-connected veterans whose annual income falls below a certain threshold, veterans receiving VA pension benefits, or Veterans eligible for Medicaid programs.

Priority Group 6: Veterans with 0% service-connected disabilities, exposed to ionizing radiation during the occupation of Hiroshima and Nagasaki, project 112/Shipboard Hazard and Defense participants, served in the Republic of Vietnam between 9 January 1962 and 7 May 1975, served in the Persian Gulf War between 2 August 1990 and 11 November 1998, served at Camp Lejeune for at least 30 days between 1 August 1953 and 31 December 1987, or who served in a theater of combat operations after 11 November 1998.

Priority Group 7: Veterans with gross household income below a certain threshold and who agree to pay copays (no Veterans in our study were in this priority group).

Priority Group 8: Veterans with gross household income above this threshold and who agree to pay copays (no Veterans in our study were in this priority group).

Table 1.

Descriptive Statistics for Patient Characteristics: Methicillin-Resistant Staphylococcus aureus Healthcare-Associated Infection on First Day of Calendar Month

CharacteristicsNo MRSA HAIMRSA HAI
No.(%)No.(%)
Total No.2675307
Age, mean (SD)71.2(12.3)71.3(11.9)
Female sex71(2.65%)6(1.95%)
Race/ethnicity
 White2049(76.60%)226(73.62%)
 Black457(17.08%)56(18.24%)
 Other/unknown/missing169(6.32%)25(8.14%)
Marital status
 Married878(32.82%)105(34.20%)
 Never married40(1.50%)(0.00%)
 Divorced846(31.63%)103(33.55%)
 Separated99(3.70%)3(0.98%)
 Widowed394(14.73%)50(16.29%)
 Unknown/missing52(1.94%)6(1.95%)
VA priority groupa
 11079(40.34%)129(42.02%)
 2186(6.95%)34(11.07%)
 3388(14.50%)40(13.03%)
 4151(5.64%)20(6.51%)
 5–6870(32.52%)84(27.36%)
Insurance
 No insurance2275(85.05%)269(87.62%)
 Insurance299(11.18%)26(8.47%)
 Missing101(3.78%)12(3.91%)
VRE infection in 365 d prior to admission104(3.89%)15(4.89%)
Comorbidity index, mean 4.03.24.43.2
Total LTCC cost prior to index date$64 837 $71 894 $70 250 $84 340
Inpatient cost in 365 d prior to admission$82 953 $152 548 $100 078 $201 254
Outpatient cost in 365 d prior to admission$17 642 $21 361 $18 541 $20 374
CharacteristicsNo MRSA HAIMRSA HAI
No.(%)No.(%)
Total No.2675307
Age, mean (SD)71.2(12.3)71.3(11.9)
Female sex71(2.65%)6(1.95%)
Race/ethnicity
 White2049(76.60%)226(73.62%)
 Black457(17.08%)56(18.24%)
 Other/unknown/missing169(6.32%)25(8.14%)
Marital status
 Married878(32.82%)105(34.20%)
 Never married40(1.50%)(0.00%)
 Divorced846(31.63%)103(33.55%)
 Separated99(3.70%)3(0.98%)
 Widowed394(14.73%)50(16.29%)
 Unknown/missing52(1.94%)6(1.95%)
VA priority groupa
 11079(40.34%)129(42.02%)
 2186(6.95%)34(11.07%)
 3388(14.50%)40(13.03%)
 4151(5.64%)20(6.51%)
 5–6870(32.52%)84(27.36%)
Insurance
 No insurance2275(85.05%)269(87.62%)
 Insurance299(11.18%)26(8.47%)
 Missing101(3.78%)12(3.91%)
VRE infection in 365 d prior to admission104(3.89%)15(4.89%)
Comorbidity index, mean 4.03.24.43.2
Total LTCC cost prior to index date$64 837 $71 894 $70 250 $84 340
Inpatient cost in 365 d prior to admission$82 953 $152 548 $100 078 $201 254
Outpatient cost in 365 d prior to admission$17 642 $21 361 $18 541 $20 374

Data are presented as No. (%) unless otherwise indicated.

Abbreviations: HAI, healthcare-associated infection; LTCC, long-term care center; MRSA, methicillin-resistant Staphylococcus aureus; SD, standard deviation; VA, Veterans Affairs; VRE, vancomycin-resistant enterococci.

aVA enrollment priority groups are defined as follows:

Priority Group 1: Veterans with service-connected disabilities 50% or more disabling or whose service-connected conditions cause them to be unemployable.

Priority Group 2: Veterans with service-connected disabilities 30%–40% disabling.

Priority Group 3: Veterans who are former prisoners of war, were awarded a Purple Heart medal, were discharged from the military due to a disability incurred or aggravated in the line of duty, with service-connected disability 10%–20% disabling, were disabled by treatment or vocational rehabilitation, or were awarded the Medal of Honor.

Priority Group 4: Veterans who are receiving aid or household benefits from VA or who are catastrophically disabled.

Priority Group 5: Nonservice-connected veterans and service-connected veterans whose annual income falls below a certain threshold, veterans receiving VA pension benefits, or Veterans eligible for Medicaid programs.

Priority Group 6: Veterans with 0% service-connected disabilities, exposed to ionizing radiation during the occupation of Hiroshima and Nagasaki, project 112/Shipboard Hazard and Defense participants, served in the Republic of Vietnam between 9 January 1962 and 7 May 1975, served in the Persian Gulf War between 2 August 1990 and 11 November 1998, served at Camp Lejeune for at least 30 days between 1 August 1953 and 31 December 1987, or who served in a theater of combat operations after 11 November 1998.

Priority Group 7: Veterans with gross household income below a certain threshold and who agree to pay copays (no Veterans in our study were in this priority group).

Priority Group 8: Veterans with gross household income above this threshold and who agree to pay copays (no Veterans in our study were in this priority group).

Figure 1 shows the unadjusted mean total costs and the percentage of patients with any acute care costs in patients with and without MRSA HAIs in the 1-month period following the index date. Mean LTCC costs during this period were similar between the 2 groups ($25 853 vs $24 102). However, the percentage of patients admitted to an acute care facility (44.0% vs 15.2%) and the mean acute care costs ($13 301 vs $3328) were substantially higher in those with MRSA HAIs compared to those without MRSA HAIs. More than two-thirds of those with sterile site infections were admitted to an acute care facility and, overall, the mean acute care costs in these patients were $22 748.

Unadjusted mean costs and percentage of patients with acute care admissions by methicillin-resistant Staphylococcus aureus (MRSA) infection status during 1 month following index date.
Figure 1.

Unadjusted mean costs and percentage of patients with acute care admissions by methicillin-resistant Staphylococcus aureus (MRSA) infection status during 1 month following index date.

Table 2 shows results of the 2-part regression models predicting 1-month acute care costs. The logistic model evaluating the probability of an acute care admission showed that MRSA HAIs increased the odds of being admitted to an acute care facility with odds ratios ranging from 3.26 (P < .0001) for those with nonsterile site infections to 11.34 (P < .0001) for those with sterile site infections. In addition, acute care costs during this period were higher for all MRSA HAI patients ($9711; P < .0001) and in those with sterile ($19 488; P < .0001) or nonsterile ($7219; P < .0001) site infections compared to those with no MRSA HAIs. When we evaluated these outcomes for patients from exposure to discharge from the LTCC facility, the results were similar. We also found consistent results when expanding the definition of MRSA HAI to include the first day of the calendar month ± 1 day (Supplementary Tables 2 and 3) and ± 2 days (Supplementary Tables 5 and 6).

Table 2.

Results From 2-Part Models Analyzing Acute Care Cost Among Patients With and Without Methicillin-Resistant Staphylococcus aureus Infection on First Day of Calendar Month (N = 2982)

Positive Culture TypePart 1 (Logistic Model)Overall Absolute Effect
ORP Value95% CIMarginal EffectP Value95% CI
LLULLLUL
Costs captured during 1 mo following index date
 Total cost
  Combined4.389<.00013.3985.669$9711<.0001$6961$12 462
  Sterile site11.340<.00016.27120.509$19 488<.0001$11 237$27 739
  Nonsterile site3.263<.00012.4684.314$7219<.0001$4552$9886
 Variable cost
  Combined4.389<.00013.3985.669$5223<.0001$3718$6727
  Sterile site11.340<.00016.27120.509$10 410<.0001$5924$14 896
  Nonsterile site3.263<.00012.4684.314$3895<.0001$2428$5361
Costs captured during all months following index date
 Total cost
  Combined3.205<.00012.4914.124$13 733 <.0001$8300 $19 167
  Sterile site10.368<.00015.11121.035$39 394 <.0001$18 800 $59 988
  Nonsterile site2.475<.00011.8943.236$7322 .001$2847 $11 797
 Variable cost
  Combined3.205<.00012.4914.124$7154 <.0001$4281 $10 028
  Sterile site10.368<.00015.11121.035$21 051 <.0001$9943 $32 158
  Nonsterile site2.475<.00011.8943.236$3696 .002$1373 $6019
Positive Culture TypePart 1 (Logistic Model)Overall Absolute Effect
ORP Value95% CIMarginal EffectP Value95% CI
LLULLLUL
Costs captured during 1 mo following index date
 Total cost
  Combined4.389<.00013.3985.669$9711<.0001$6961$12 462
  Sterile site11.340<.00016.27120.509$19 488<.0001$11 237$27 739
  Nonsterile site3.263<.00012.4684.314$7219<.0001$4552$9886
 Variable cost
  Combined4.389<.00013.3985.669$5223<.0001$3718$6727
  Sterile site11.340<.00016.27120.509$10 410<.0001$5924$14 896
  Nonsterile site3.263<.00012.4684.314$3895<.0001$2428$5361
Costs captured during all months following index date
 Total cost
  Combined3.205<.00012.4914.124$13 733 <.0001$8300 $19 167
  Sterile site10.368<.00015.11121.035$39 394 <.0001$18 800 $59 988
  Nonsterile site2.475<.00011.8943.236$7322 .001$2847 $11 797
 Variable cost
  Combined3.205<.00012.4914.124$7154 <.0001$4281 $10 028
  Sterile site10.368<.00015.11121.035$21 051 <.0001$9943 $32 158
  Nonsterile site2.475<.00011.8943.236$3696 .002$1373 $6019

Multivariable models assumed a gamma distribution and a log link function and controlled for the following covariates: age, sex, race, marital status, Veterans Affairs priority group, insurance, vancomycin-resistant Enterococcus infection during 365 days prior to admission, Clostridioides difficile infection during 365 days prior to admission, total long-term care center cost. Aside from those who had died (7.7%), all Veterans had at least 1 month of follow-up time following index date over which costs could accrue.

Abbreviations: CI, confidence interval; LL, lower limit; OR, odds ratio; UL, upper limit.

Table 2.

Results From 2-Part Models Analyzing Acute Care Cost Among Patients With and Without Methicillin-Resistant Staphylococcus aureus Infection on First Day of Calendar Month (N = 2982)

Positive Culture TypePart 1 (Logistic Model)Overall Absolute Effect
ORP Value95% CIMarginal EffectP Value95% CI
LLULLLUL
Costs captured during 1 mo following index date
 Total cost
  Combined4.389<.00013.3985.669$9711<.0001$6961$12 462
  Sterile site11.340<.00016.27120.509$19 488<.0001$11 237$27 739
  Nonsterile site3.263<.00012.4684.314$7219<.0001$4552$9886
 Variable cost
  Combined4.389<.00013.3985.669$5223<.0001$3718$6727
  Sterile site11.340<.00016.27120.509$10 410<.0001$5924$14 896
  Nonsterile site3.263<.00012.4684.314$3895<.0001$2428$5361
Costs captured during all months following index date
 Total cost
  Combined3.205<.00012.4914.124$13 733 <.0001$8300 $19 167
  Sterile site10.368<.00015.11121.035$39 394 <.0001$18 800 $59 988
  Nonsterile site2.475<.00011.8943.236$7322 .001$2847 $11 797
 Variable cost
  Combined3.205<.00012.4914.124$7154 <.0001$4281 $10 028
  Sterile site10.368<.00015.11121.035$21 051 <.0001$9943 $32 158
  Nonsterile site2.475<.00011.8943.236$3696 .002$1373 $6019
Positive Culture TypePart 1 (Logistic Model)Overall Absolute Effect
ORP Value95% CIMarginal EffectP Value95% CI
LLULLLUL
Costs captured during 1 mo following index date
 Total cost
  Combined4.389<.00013.3985.669$9711<.0001$6961$12 462
  Sterile site11.340<.00016.27120.509$19 488<.0001$11 237$27 739
  Nonsterile site3.263<.00012.4684.314$7219<.0001$4552$9886
 Variable cost
  Combined4.389<.00013.3985.669$5223<.0001$3718$6727
  Sterile site11.340<.00016.27120.509$10 410<.0001$5924$14 896
  Nonsterile site3.263<.00012.4684.314$3895<.0001$2428$5361
Costs captured during all months following index date
 Total cost
  Combined3.205<.00012.4914.124$13 733 <.0001$8300 $19 167
  Sterile site10.368<.00015.11121.035$39 394 <.0001$18 800 $59 988
  Nonsterile site2.475<.00011.8943.236$7322 .001$2847 $11 797
 Variable cost
  Combined3.205<.00012.4914.124$7154 <.0001$4281 $10 028
  Sterile site10.368<.00015.11121.035$21 051 <.0001$9943 $32 158
  Nonsterile site2.475<.00011.8943.236$3696 .002$1373 $6019

Multivariable models assumed a gamma distribution and a log link function and controlled for the following covariates: age, sex, race, marital status, Veterans Affairs priority group, insurance, vancomycin-resistant Enterococcus infection during 365 days prior to admission, Clostridioides difficile infection during 365 days prior to admission, total long-term care center cost. Aside from those who had died (7.7%), all Veterans had at least 1 month of follow-up time following index date over which costs could accrue.

Abbreviations: CI, confidence interval; LL, lower limit; OR, odds ratio; UL, upper limit.

Table 3 shows the results from multivariable regression models for LTCC costs alone and the combined acute care and LTCC outcome. We found no difference in LTCC costs between patients with and without MRSA HAIs whether for costs in the 1 month following the index date ($884; P = .317) or for costs over the remainder of the patient’s stay following the index date ($10 644; P = .636). We did find a significant difference in combined LTCC and acute care costs in the 1-month period following index date ($11 196; P < .0001), but there was no significant effect over the entire post–index period ($29 343; P = .210).

Table 3.

Results From Generalized Linear Regression Models Analyzing 30-Day Costs Among Patients With and Without Methicillin-Resistant Staphylococcus aureus Infection on First Day of Calendar Month (N = 2982)

Positive Culture TypeLong-term CareLong-term Care and Acute Care Combined
Marginal EffectP Value95% CIMarginal EffectP Value95% CI
LLULLLUL
Costs captured during 1 mo following index date
 Total cost
  Combined$884.317–$846$2614$11 196 <.0001$8021 $14 371
  Sterile site–$908.626–$4559$2744$17 775 <.0001$10 520 $25 031
  Nonsterile site$1260.198–$658$3178$9342 <.0001$5939 $12 745
 Variable cost
  Combined$542.239–$360$1445$6067 <.0001$4350 $7784
  Sterile site–$247.796–$2119$1626$9796 <.0001$5832 $13 759
  Nonsterile site$745.148–$265$1755$5072 <.0001$3231 $6914
Costs captured during all months following index date
 Total cost
  Combined$10 644.636–$33 444$54 732$29 343.210–$16 515$75 200
  Sterile site$45 788.440–$70 554$162 130$87 501.154–$32 740$207 742
  Nonsterile site$1093.962–$44 312$46 497$13 646.571–$33 526$60 819
 Variable cost
  Combined$5270.636–$16 577$27 117$14 808.203–$7970$37 585
  Sterile site$25 358.407–$34 531$85 247$47 526.135–$14 722$109 774
  Nonsterile site$179.987–$22 030$22 387$6389.588–$16 713$29 490
Positive Culture TypeLong-term CareLong-term Care and Acute Care Combined
Marginal EffectP Value95% CIMarginal EffectP Value95% CI
LLULLLUL
Costs captured during 1 mo following index date
 Total cost
  Combined$884.317–$846$2614$11 196 <.0001$8021 $14 371
  Sterile site–$908.626–$4559$2744$17 775 <.0001$10 520 $25 031
  Nonsterile site$1260.198–$658$3178$9342 <.0001$5939 $12 745
 Variable cost
  Combined$542.239–$360$1445$6067 <.0001$4350 $7784
  Sterile site–$247.796–$2119$1626$9796 <.0001$5832 $13 759
  Nonsterile site$745.148–$265$1755$5072 <.0001$3231 $6914
Costs captured during all months following index date
 Total cost
  Combined$10 644.636–$33 444$54 732$29 343.210–$16 515$75 200
  Sterile site$45 788.440–$70 554$162 130$87 501.154–$32 740$207 742
  Nonsterile site$1093.962–$44 312$46 497$13 646.571–$33 526$60 819
 Variable cost
  Combined$5270.636–$16 577$27 117$14 808.203–$7970$37 585
  Sterile site$25 358.407–$34 531$85 247$47 526.135–$14 722$109 774
  Nonsterile site$179.987–$22 030$22 387$6389.588–$16 713$29 490

Multivariable models assumed a gamma distribution and a log link function and controlled for the following covariates: age, sex, race, marital status, Veterans Affairs priority group, insurance, vancomycin-resistant Enterococcus infection during 365 days prior to admission, total long-term care center cost prior to index date (date of methicillin-resistant Staphylococcus aureus healthcare-associated infection). Aside from those who had died (7.7%), all Veterans had at least 1 month of follow-up time following index date over which costs could accrue.

Abbreviations: CI, confidence interval; LL, lower limit; OR, odds ratio; UL, upper limit.

Table 3.

Results From Generalized Linear Regression Models Analyzing 30-Day Costs Among Patients With and Without Methicillin-Resistant Staphylococcus aureus Infection on First Day of Calendar Month (N = 2982)

Positive Culture TypeLong-term CareLong-term Care and Acute Care Combined
Marginal EffectP Value95% CIMarginal EffectP Value95% CI
LLULLLUL
Costs captured during 1 mo following index date
 Total cost
  Combined$884.317–$846$2614$11 196 <.0001$8021 $14 371
  Sterile site–$908.626–$4559$2744$17 775 <.0001$10 520 $25 031
  Nonsterile site$1260.198–$658$3178$9342 <.0001$5939 $12 745
 Variable cost
  Combined$542.239–$360$1445$6067 <.0001$4350 $7784
  Sterile site–$247.796–$2119$1626$9796 <.0001$5832 $13 759
  Nonsterile site$745.148–$265$1755$5072 <.0001$3231 $6914
Costs captured during all months following index date
 Total cost
  Combined$10 644.636–$33 444$54 732$29 343.210–$16 515$75 200
  Sterile site$45 788.440–$70 554$162 130$87 501.154–$32 740$207 742
  Nonsterile site$1093.962–$44 312$46 497$13 646.571–$33 526$60 819
 Variable cost
  Combined$5270.636–$16 577$27 117$14 808.203–$7970$37 585
  Sterile site$25 358.407–$34 531$85 247$47 526.135–$14 722$109 774
  Nonsterile site$179.987–$22 030$22 387$6389.588–$16 713$29 490
Positive Culture TypeLong-term CareLong-term Care and Acute Care Combined
Marginal EffectP Value95% CIMarginal EffectP Value95% CI
LLULLLUL
Costs captured during 1 mo following index date
 Total cost
  Combined$884.317–$846$2614$11 196 <.0001$8021 $14 371
  Sterile site–$908.626–$4559$2744$17 775 <.0001$10 520 $25 031
  Nonsterile site$1260.198–$658$3178$9342 <.0001$5939 $12 745
 Variable cost
  Combined$542.239–$360$1445$6067 <.0001$4350 $7784
  Sterile site–$247.796–$2119$1626$9796 <.0001$5832 $13 759
  Nonsterile site$745.148–$265$1755$5072 <.0001$3231 $6914
Costs captured during all months following index date
 Total cost
  Combined$10 644.636–$33 444$54 732$29 343.210–$16 515$75 200
  Sterile site$45 788.440–$70 554$162 130$87 501.154–$32 740$207 742
  Nonsterile site$1093.962–$44 312$46 497$13 646.571–$33 526$60 819
 Variable cost
  Combined$5270.636–$16 577$27 117$14 808.203–$7970$37 585
  Sterile site$25 358.407–$34 531$85 247$47 526.135–$14 722$109 774
  Nonsterile site$179.987–$22 030$22 387$6389.588–$16 713$29 490

Multivariable models assumed a gamma distribution and a log link function and controlled for the following covariates: age, sex, race, marital status, Veterans Affairs priority group, insurance, vancomycin-resistant Enterococcus infection during 365 days prior to admission, total long-term care center cost prior to index date (date of methicillin-resistant Staphylococcus aureus healthcare-associated infection). Aside from those who had died (7.7%), all Veterans had at least 1 month of follow-up time following index date over which costs could accrue.

Abbreviations: CI, confidence interval; LL, lower limit; OR, odds ratio; UL, upper limit.

Discussion

This is the first study to assess the attributable cost of MRSA HAIs among LTCC patients. We found that increases in overall cost were driven by increases in both the odds of being transferred to an acute care facility and costs in acute care settings while LTCC costs were not significantly different between patients with and without MRSA HAIs. Compared to patients without MRSA HAIs, the odds of being transferred to an acute care facility were elevated both for patients with sterile and nonsterile site HAIs, although the magnitude of this effect was much higher in those with sterile site HAIs. For HAIs from nonsterile sites, the estimates of attributable acute care cost were virtually identical when costs were captured over the entire post-HAI time period ($7322 for total cost) compared to just the first month following the infection ($7219 for total cost), indicating that greater resources are needed for caring for these patients only within the first month following infection. For HAIs from sterile sites, on the other hand, the attributable cost estimate was roughly twice as large when considering the entire post-HAI time period ($39 394 for total cost) compared to just the first month following infection ($19 488 for total cost). This suggests that the increased intensity of care required for patients with these infections may last beyond this first month.

Our finding of an elevated risk of transfer to an acute care facility for LTCC patients with MRSA HAIs has important ramifications for transmission of MRSA. Interhospital patient transfer has been identified as a possible mechanism for the spread of infectious organisms [27–29]. Communication of the patient’s MRSA status between the sending and receiving facility and proper precautionary infection control practices such as isolation, contact precautions, and proper hand hygiene when caring for the transferred patient in the acute care facility are critical for preventing transmission.

That we did not find evidence of increased costs in LTCCs following MRSA HAIs is perhaps not surprising given the significant increase in length of stay associated with infections in healthcare settings found by many previous studies [10, 11]. Patients in LTCCs will be staying in those facilities for a long period of time—months or even years—regardless of whether they acquire an infection. So a temporary and time-varying condition such as a MRSA HAI will not impact the duration of care for patients in a LTCC facility.

While this is the first study to estimate the cost of HAIs among LTCC patients, we have published several similar estimates for patients admitted to VA acute care facilities using the same cost dataset, making comparisons possible. One of these estimated the attributable cost of MRSA HAIs in acute care facilities in both sterile and nonsterile sites combined to be $24 015, roughly twice as large as our estimate of $13 733 when capturing costs over the entire post-HAI period [10]. A subsequent study estimated the cost of HAIs due to gram-negative bacteria to be $13 744–$12 050 depending on the number of drug classes to which the organism was resistant [11].

Our study had several limitations. First, the exposure variable in our statistical analyses was a positive clinical culture for one of several MDR organisms. From our administrative data, it was not possible to definitively say whether these cultures were true infections. However, we identified whether the cultures were obtained from a site that is usually considered sterile (blood, cerebrospinal fluid, pleural fluid, and synovial fluid) or nonsterile. Positive cultures from sterile sites are much more likely to be from true infections, rather than colonization. Second, our analyses used data from a large administrative dataset. These data were not produced for the purposes of research but were collected in the process of providing care to patients. In addition, the patient population (older and predominantly male) and financial model (reliant on federal tax dollars rather than third-party payers) of the VA Health System are quite different than other health systems in the US. This means that these results may not be generalizable to other settings to the extent that differences exist between patients and healthcare delivery systems. In addition, while we controlled for a number of observable characteristics that would increase the risk of both an HAI and mortality—including comorbidity index, surgery, ICU admissions, and the cost of previous healthcare encounters—it is possible that residual confounding remains. Finally, while we were able to track movement of the patients in our study between VA facilities, we do not have data on any care they received at non-VA facilities. If LTCC patients with MRSA HAIs are at increased risk for transfer to non-VA acute care facilities, then our estimates of the attributable cost of these infections may be underestimated.

In conclusion, in a cohort of patients admitted to a VA LTCC, we found that MRSA HAIs lead to an increased risk of transfer to an acute care facility and higher acute care costs. However, there was no significant effect on LTCC costs.

Supplementary Data

Supplementary materials are available at Clinical Infectious Diseases online. Consisting of data provided by the authors to benefit the reader, the posted materials are not copyedited and are the sole responsibility of the authors, so questions or comments should be addressed to the corresponding author.

Notes

Acknowledgments. We would like to acknowledge funding for this supplement from the Informatics, Decision-Enhancement and Analytic Sciences (IDEAS) Center and the VA Health Services Research and Development (HSR&D) Service.

Disclaimer. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Department of Veterans Affairs (VA).

Financial support. This work was supported with the use of facilities and resources at the George E. Wahlen VA Medical Center, Salt Lake City, Utah. This study was supported by the Agency for Healthcare Research and Quality (grant number R01 HS023794 to E. L.); the VA Health Services Research and Development Service (Center of Innovation: Informatics, Decision-Enhancement, and Analytic Sciences [IDEAS] Center) (CIN 13–414 to R. E. N., M. J., and V. W. S.); and the Centers for Disease Control and Prevention Cooperative Agreement (FOA number CK000163 to E. L.) Epicenters for the Prevention of Healthcare Associated Infections.

Supplement sponsorship. This supplement is sponsored by the Informatics, Decision-Enhancement and Analytic Sciences (IDEAS) Center.

Potential conflicts of interest. M. D. has been a consultant to GlaxoSmithKline plc and Baxter International Inc. J. A. D. reports serving as a consultant and/or advisory board member for Allergan, Boehringer Ingelheim, Catabasis, Ironwood Pharmaceuticals, Janssen, Kite Pharma, MeiraGTx, Merck, Otsuka, Regeneron, Sarepta, Sage Therapeutics, Sanofi, Takeda, The Medicines Company, and Vertex and has received research funding from AbbVie, Biogen, Humana, Janssen, Novartis, Pfizer, PhRMA, Regeneron, Sanofi, and Valeant, all unrelated to this study. All other authors report no potential conflicts.

All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

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