Abstract

Background

Regions are considering the use of electronic registries to track patients who carry antibiotic-resistant bacteria, including carbapenem-resistant Enterobacteriaceae (CRE). Implementing such a registry can be challenging and requires time, effort, and resources; therefore, there is a need to better understand the potential impact.

Methods

We developed an agent-based model of all inpatient healthcare facilities (90 acute care hospitals, 9 long-term acute care hospitals, 351 skilled nursing facilities, and 12 ventilator-capable skilled nursing facilities) in the Chicago metropolitan area, surrounding communities, and patient flow using our Regional Healthcare Ecosystem Analyst software platform. Scenarios explored the impact of a registry that tracked patients carrying CRE to help guide infection prevention and control.

Results

When all Illinois facilities participated (n = 402), the registry reduced the number of new carriers by 11.7% and CRE prevalence by 7.6% over a 3-year period. When 75% of the largest Illinois facilities participated (n = 304), registry use resulted in a 11.6% relative reduction in new carriers (16.9% and 1.2% in participating and nonparticipating facilities, respectively) and 5.0% relative reduction in prevalence. When 50% participated (n = 201), there were 10.7% and 5.6% relative reductions in incident carriers and prevalence, respectively. When 25% participated (n = 101), there was a 9.1% relative reduction in incident carriers (20.4% and 1.6% in participating and nonparticipating facilities, respectively) and 2.8% relative reduction in prevalence.

Conclusions

Implementing an extensively drug-resistant organism registry reduced CRE spread, even when only 25% of the largest Illinois facilities participated due to patient sharing. Nonparticipating facilities garnered benefits, with reductions in new carriers.

Regions concerned about the spread of extensively drug-resistant organisms (XDROs) [1–3] have considered building and using electronic registries that can track which patients are carrying antibiotic-resistant bacteria and can alert healthcare facilities about these patients when they are admitted. Implementing such registries can require time, effort, and resources; therefore, there is a need to better understand how such registries may improve the control of the spread of XDROs such as carbapenem-resistant Enterobacteriaceae (CRE). Antibiotic-resistant organisms are a major public health problem [4], with infections resulting in substantial morbidity, mortality, and added costs [5–8]. Our previous work has demonstrated that extensive patient movement and sharing occurs among healthcare facilities in a region [9, 10] and that outbreaks of antibiotic-resistant bacteria such as methicillin-resistant Staphylococcus aureus (MRSA) [11–13], CRE [14–16], and vancomycin-resistant enterococci [12] could readily spread to many other facilities. However, without a centralized registry showing which patients may be carrying such bacteria, facilities may be unaware of a patient’s carrier status upon admission and therefore may not take appropriate measures, such as contact precautions, to contain pathogen spread and prevent and control outbreaks. By providing actionable data directly to healthcare providers, a registry that could track those patients who are carrying XDROs could forewarn healthcare facilities to take the appropriate infection control measures when one of those patients is admitted to their facilities.

While a registry may bring a number of benefits, there are accompanying questions and challenges. For example, since getting all facilities in a region to participate can be challenging, it would be helpful to know how many facilities need to participate in a registry to make it worthwhile. Do nonparticipating facilities still garner benefits? The eventual impact of an XDRO registry is difficult to estimate as its impact may be far reaching. Before implementing such a registry, policy makers (eg, public health entities, health commissioners, mayors, hospital administrators, heads of infection control) may have several questions: Should a state or region implement an XDRO registry? What is its impact on pathogen spread? How would variation in facility participation impact its effectiveness? To answer these questions, we used our Regional Healthcare Ecosystem Analyst (RHEA) software to develop a model of all the healthcare facilities in the greater Chicago region, and to simulate what would happen to CRE with the introduction and use of an XDRO registry vs having no registry.

METHODS

Using our previously described RHEA software [17], we developed an agent-based model of the Chicago metropolitan area, the third most populous region in the United States. RHEA:Chicago consists of 462 total healthcare facilities: 90 acute care hospitals, 9 long-term acute care hospitals (LTACHs), 351 skilled nursing facilities (SNFs), and 12 ventilator-capable skilled nursing facilities (vSNFs; specialized skilled nursing facilities capable of caring for patients dependent on mechanical ventilation [18]). These facilities serve 9.9 million people across 10 800 square miles covering parts of Illinois (402 facilities), Wisconsin (11 facilities), and Indiana (49 facilities). The Supplementary Materials describe Illinois’ XDRO registry and our data sources, and Supplementary Table 1 lists the model input parameters and values.

RHEA:Chicago Model

In brief, the model represents each patient as a computational agent, which on a given day, can either carry (ie, infected or colonized) or not carry CRE. Each simulated day, agents move from the community or other healthcare facilities into various healthcare facilities in the Chicago metropolitan region. Each virtual healthcare facility has a number of beds (based on actual bed count). Hospitals consist of multiple units (general units and intensive care units), LTACHs consist of long-term units, vSNFs consist of ventilated, skilled, and other units, and SNFs consist of a single large unit (representing the high degree of social interactions among residents). Once a patient is admitted to a facility, a probability draw determines which of that facility’s units the patient enters and a draw from that facility- and unit-specific length-of-stay (LOS) distribution determines how long the patient will remain in the unit and facility. CRE carriers have an additional LOS, staying 3.75 and 9.0 days longer in hospitals and LTACHs, respectively, based on actual data. Within each unit, patients mix homogeneously, and CRE carriers can transmit to noncarriers, based on a unit- and facility-specific transmission coefficient (β): β × susceptible patients × infectious patients. Once the patient’s LOS elapses, the patient leaves the facility and has probabilities of returning to the community, directly transferring to another facility, or returning to the community for a period before being readmitted to the same or another facility. Upon discharge, CRE carriers had a 2-fold increased risk of readmission within 365 days; those discharged from a hospital general unit and an LTACH had a higher chance of transferring to an LTACH and a vSNF ventilated floor, respectively (Supplementary Table 1).

In the absence of a registry, only a fraction of CRE carriers would be detected, based on the percentage of CRE carriers identified by clinical cultures (12%, Supplementary Table 1). Those patients known to be CRE positive are placed under contact precautions (ie, a single room and use of gloves and gowns by staff on room entry) on admission for their LOS duration in hospitals, LTACHs, and vSNFs, and for 10 days in SNFs (representing symptom-based contact precautions applied for infection). Patients under contact precautions had a probability of remaining so upon transfer to other facilities (based on the likelihood of interfacility communication) and when readmitted to the same facility (Supplementary Table 1). In addition, a fraction of non-CRE carriers and unknown CRE carriers were placed under contact precautions for other reasons (eg, MRSA colonization), varying by facility type (Supplementary Table 1). Contact precautions attenuated transmission by 40%, a combination of the intervention’s efficacy and healthcare staff compliance.

We modeled the use of an XDRO registry, which serves to increase the fraction of all CRE carriers identified by facility type based on an electronic public health registry. On admission, healthcare staff searched for each patient in the registry to identify if they are a known CRE carrier. If identified as CRE positive, the patient was placed under contact precautions, as described above. Upon discharge, staff added newly identified carriers to the registry.

Scenarios and Experiments

Our baseline scenario assumed no CRE-specific intervention and no existing registry while our intervention scenarios consist of introducing and using an XDRO registry under different circumstances. As this is a state-based registry, only Illinois facilities were eligible to participate and facilities in Wisconsin and Indiana, though part of the RHEA:Chicago model, could not use the registry. The registry was implemented in a proportion of eligible facilities, ranked by facility bed size. Sensitivity analyses varied the proportion of eligible facilities participating and using the registry (25%–100%) and the fraction of all carriers in the registry (40%–80%). Each simulation experiment consisted of running the model 50 times and simulated 3 years. The intervention impact was the difference between XDRO registry scenarios and the baseline scenario.

RESULTS

No XDRO Registry

Figure 1 shows the CRE prevalence among currently admitted patients in all healthcare facilities regionwide over time to be 1.54% (interquartile range, 1.47%–1.60%) at year 3. Table 1 shows the cumulative number of new CRE carriers (ie, number of patients who acquired CRE since simulation start) over time with no XDRO registry. Over the 3-year period there would be 12 735 new CRE carriers regionwide, with most (60%; 7639 new carriers) occurring in hospitals, and of those, 1609 occur in intensive care units (13% of total); 3841 and 1152 occur in LTACHs and vSNF ventilated units, respectively.

Table 1.

Cumulative Number of New Carbapenem-resistant Enterobacteriaceae (CRE) Carriers Regionwide at Given Points in Time With and Without the Use of an Extensively Drug-resistant Organism Registry (XDRO; With 60% of All Carriers in the Registry) in Various Groupings of Healthcare Facilities and Cumulative Number of Averted Incident Carriers

Registry ParticipationTime, mo
061218243036
Cumulative No. of incident CRE carriers, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities10 (9–13)1922 (1741–2055)3718 (3507–4051)5569 (5163–5946)7469 (6923–7806)9398 (8537–9814)11 244 (10 295–11 819)
 75% of IL facilities11 (8–13)2019 (1849–2156)3814 (3636–4121)5755 (5360–6024)7518 (7200–8020)9445 (9021–10 092)11 262 (10 818–12 112)
 50% of IL facilities12 (9–14)2034 (1860–2121)3973 (3575–4214)5870 (5377–6268)7697 (7004–8331)9446 (8795–10 453)11 377 (10 518–12 455)
 25% of IL facilities10 (8–13)1979 (1832–2196)3917 (3692–4267)5944 (5331–6331)7906 (7136–8517)9637 (8931–10 564)11 570 (10 875–12 623)
Cumulative No. of averted incident CRE carriers compared to no XDRO registry use, median
 100% of IL facilities176460747102412171491
 75% of IL facilities7936456197511701473
 50% of IL facilities6420544679611691358
 25% of IL facilities1192613725879781165
Registry ParticipationTime, mo
061218243036
Cumulative No. of incident CRE carriers, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities10 (9–13)1922 (1741–2055)3718 (3507–4051)5569 (5163–5946)7469 (6923–7806)9398 (8537–9814)11 244 (10 295–11 819)
 75% of IL facilities11 (8–13)2019 (1849–2156)3814 (3636–4121)5755 (5360–6024)7518 (7200–8020)9445 (9021–10 092)11 262 (10 818–12 112)
 50% of IL facilities12 (9–14)2034 (1860–2121)3973 (3575–4214)5870 (5377–6268)7697 (7004–8331)9446 (8795–10 453)11 377 (10 518–12 455)
 25% of IL facilities10 (8–13)1979 (1832–2196)3917 (3692–4267)5944 (5331–6331)7906 (7136–8517)9637 (8931–10 564)11 570 (10 875–12 623)
Cumulative No. of averted incident CRE carriers compared to no XDRO registry use, median
 100% of IL facilities176460747102412171491
 75% of IL facilities7936456197511701473
 50% of IL facilities6420544679611691358
 25% of IL facilities1192613725879781165

Only facilities in the Chicago region within the state of Illinois were eligible to participate in the XDRO registry—100% of eligible facilities: 402 facilities and 64 022 total beds; 75% of eligible facilities: 304 facilities and 57 022 beds (89% of total eligible); 50% of eligible facilities: 201 facilities and 44 382 beds (69% of total eligible); 25% of eligible facilities: 101 facilities and 27 232 beds (43% of total eligible).

Abbreviations: CRE, carbapenem-resistant Enterobacteriaceae; IL, Illinois; IQR, interquartile range; XDRO, extensively drug-resistant organism.

Table 1.

Cumulative Number of New Carbapenem-resistant Enterobacteriaceae (CRE) Carriers Regionwide at Given Points in Time With and Without the Use of an Extensively Drug-resistant Organism Registry (XDRO; With 60% of All Carriers in the Registry) in Various Groupings of Healthcare Facilities and Cumulative Number of Averted Incident Carriers

Registry ParticipationTime, mo
061218243036
Cumulative No. of incident CRE carriers, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities10 (9–13)1922 (1741–2055)3718 (3507–4051)5569 (5163–5946)7469 (6923–7806)9398 (8537–9814)11 244 (10 295–11 819)
 75% of IL facilities11 (8–13)2019 (1849–2156)3814 (3636–4121)5755 (5360–6024)7518 (7200–8020)9445 (9021–10 092)11 262 (10 818–12 112)
 50% of IL facilities12 (9–14)2034 (1860–2121)3973 (3575–4214)5870 (5377–6268)7697 (7004–8331)9446 (8795–10 453)11 377 (10 518–12 455)
 25% of IL facilities10 (8–13)1979 (1832–2196)3917 (3692–4267)5944 (5331–6331)7906 (7136–8517)9637 (8931–10 564)11 570 (10 875–12 623)
Cumulative No. of averted incident CRE carriers compared to no XDRO registry use, median
 100% of IL facilities176460747102412171491
 75% of IL facilities7936456197511701473
 50% of IL facilities6420544679611691358
 25% of IL facilities1192613725879781165
Registry ParticipationTime, mo
061218243036
Cumulative No. of incident CRE carriers, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities10 (9–13)1922 (1741–2055)3718 (3507–4051)5569 (5163–5946)7469 (6923–7806)9398 (8537–9814)11 244 (10 295–11 819)
 75% of IL facilities11 (8–13)2019 (1849–2156)3814 (3636–4121)5755 (5360–6024)7518 (7200–8020)9445 (9021–10 092)11 262 (10 818–12 112)
 50% of IL facilities12 (9–14)2034 (1860–2121)3973 (3575–4214)5870 (5377–6268)7697 (7004–8331)9446 (8795–10 453)11 377 (10 518–12 455)
 25% of IL facilities10 (8–13)1979 (1832–2196)3917 (3692–4267)5944 (5331–6331)7906 (7136–8517)9637 (8931–10 564)11 570 (10 875–12 623)
Cumulative No. of averted incident CRE carriers compared to no XDRO registry use, median
 100% of IL facilities176460747102412171491
 75% of IL facilities7936456197511701473
 50% of IL facilities6420544679611691358
 25% of IL facilities1192613725879781165

Only facilities in the Chicago region within the state of Illinois were eligible to participate in the XDRO registry—100% of eligible facilities: 402 facilities and 64 022 total beds; 75% of eligible facilities: 304 facilities and 57 022 beds (89% of total eligible); 50% of eligible facilities: 201 facilities and 44 382 beds (69% of total eligible); 25% of eligible facilities: 101 facilities and 27 232 beds (43% of total eligible).

Abbreviations: CRE, carbapenem-resistant Enterobacteriaceae; IL, Illinois; IQR, interquartile range; XDRO, extensively drug-resistant organism.

Carbapenem-resistant Enterobacteriaceae (CRE) prevalence in healthcare facilities regionwide over time when different proportions of the largest facilities in Illinois (IL) participate and use an extensively drug-resistant organism (XDRO) registry (assumes 60% of all CRE carriers are in the XDRO registry).
Figure 1.

Carbapenem-resistant Enterobacteriaceae (CRE) prevalence in healthcare facilities regionwide over time when different proportions of the largest facilities in Illinois (IL) participate and use an extensively drug-resistant organism (XDRO) registry (assumes 60% of all CRE carriers are in the XDRO registry).

One Hundred Percent of State Healthcare Facilities Participating and Utilizing the XDRO Registry

When all Illinois facilities used a registry (n = 402: 75 hospitals, 8 LTACHs, 10 vSNFs, 309 SNFs; 64 022 total beds), regionwide CRE prevalence in healthcare facilities dropped by a relative 7.6% (compared to baseline) after 3 years of use to 1.42% (Figure 1). Over the 3-year period, registry use resulted in 1491 fewer incident carriers (11.7% relative decrease; Table 1 and Figure 2) and 88 646 additional contact precaution days. All unit types except SNFs had fewer incident carriers when using the registry; SNFs had no change. Hospitals experienced the largest relative reductions in new carriers (15.6%), followed by vSNFs (13.7%) and LTACHs (8.3%). Figure 3 shows the direct and indirect impacts of a registry (60% of carriers identified) on the relative reduction in new carriers compared to no registry. Within Illinois (ie, participating facilities), there would be a 9.4% relative reduction in CRE prevalence and 1555 fewer incident carriers (15.4% relative decrease; Figure 3). Neighboring facilities ineligible for the XDRO registry (ie, those in Indiana and Wisconsin) experienced a 4.3% relative decrease in prevalence and 103 fewer incident carriers (Figure 3).

Impact of the proportion of Illinois healthcare facilities participating and utilizing an extensively drug-resistant organism (XDRO) registry (60% of all carriers in the registry) on the cumulative number of new carbapenem-resistant Enterobacteriaceae (CRE) carriers regionwide (transmission events) over 3 simulated years. Box represents the interquartile range (25th and 75th percentile), the central line in each box is the median, whiskers are the minimum and maximum. Only facilities in the Chicago region within the state of Illinois were eligible to participate in the XDRO registry (100%: 402 facilities and 64 022 total beds; 75%: 304 facilities and 57 022 beds; 50%: 201 facilities and 44 382 beds; 25%: 101 facilities and 27 232 beds).
Figure 2.

Impact of the proportion of Illinois healthcare facilities participating and utilizing an extensively drug-resistant organism (XDRO) registry (60% of all carriers in the registry) on the cumulative number of new carbapenem-resistant Enterobacteriaceae (CRE) carriers regionwide (transmission events) over 3 simulated years. Box represents the interquartile range (25th and 75th percentile), the central line in each box is the median, whiskers are the minimum and maximum. Only facilities in the Chicago region within the state of Illinois were eligible to participate in the XDRO registry (100%: 402 facilities and 64 022 total beds; 75%: 304 facilities and 57 022 beds; 50%: 201 facilities and 44 382 beds; 25%: 101 facilities and 27 232 beds).

Relative reduction (%) in the total number of incident carbapenem-resistant Enterobacteriaceae (CRE) carriers over a 3-year period when using an extensively drug-resistant organism (XDRO) registry (60% of all CRE carriers are in the registry) compared to no XDRO registry when varying Illinois healthcare facility participation. “Participating facilities” shows the direct impact, or the reduction occurring in those facilities that participate and use the registry compared to when they did not. “Nonparticipating facilities” shows the indirect impact, or the reduction occurring in those facilities that do not participate in the registry. Only facilities in the Chicago region within the state of Illinois were eligible to participate in the XDRO registry (100%: 402 facilities and 64 022 total beds; 75%: 304 facilities and 57 022 beds; 50%: 201 facilities and 44 382 beds; 25%: 101 facilities and 27 232 beds). Nonparticipating facilities in the 100% of Illinois facilities scenario are those healthcare facilities in Indiana and Wisconsin that were not eligible to participate in the registry.
Figure 3.

Relative reduction (%) in the total number of incident carbapenem-resistant Enterobacteriaceae (CRE) carriers over a 3-year period when using an extensively drug-resistant organism (XDRO) registry (60% of all CRE carriers are in the registry) compared to no XDRO registry when varying Illinois healthcare facility participation. “Participating facilities” shows the direct impact, or the reduction occurring in those facilities that participate and use the registry compared to when they did not. “Nonparticipating facilities” shows the indirect impact, or the reduction occurring in those facilities that do not participate in the registry. Only facilities in the Chicago region within the state of Illinois were eligible to participate in the XDRO registry (100%: 402 facilities and 64 022 total beds; 75%: 304 facilities and 57 022 beds; 50%: 201 facilities and 44 382 beds; 25%: 101 facilities and 27 232 beds). Nonparticipating facilities in the 100% of Illinois facilities scenario are those healthcare facilities in Indiana and Wisconsin that were not eligible to participate in the registry.

Table 2 shows the cumulative number of new carriers over time when varying the fraction of carriers in the XDRO registry. Using the registry resulted in a 9.4% and 15.5% relative decrease in new carriers compared to no registry when 40% and 80% of all carriers were in the registry, respectively, over the 3-year period. Regionwide prevalence decreased to 1.37% (10.8% relative reduction) when 80% of carriers were identified.

Table 2.

Cumulative Number of Incident Carbapenem-resistant Enterobacteriaceae (CRE) Carriers Regionwide at Given Points in Time With and Without the Use of an Extensively Drug-resistant Organism (XDRO) Registry, Varying the Percentage of CRE Carriers Identified With Registry Use, in Various Groupings of Healthcare Facilities

Registry ParticipationTime, mo
061218243036
40% of CRE carriers in the XDRO registry, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities11 (9–14)2008 (1816–2153)3877 (3609–4145)5835 (5467–6187)7710 (7298–8131)9585 (9107–10 088)11 532 (10 970–12 152)
 75% of IL facilities10 (8–13)2013 (1854–2114)3919 (3669–4129)5838 (5429–6176)7794 (7292–8361)9678 (9072–10 599)11 637 (10 972–12 805)
 50% of IL facilities12 (10–15)1980 (1911–2147)3969 (3770–4202)5926 (5574–6303)7855 (7448–8467)9943 (9299–10 665)11 955 (11 141–12 912)
 25% of IL facilities11 (9–14)2002 (1847–2170)3987 (3701–4210)5893 (5510–6409)7761 (7339–8514)9731 (9217–10 583)11 806 (11 211–12 673)
80% of CRE carriers in the XDRO registry, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities11 (8–14)1905 (1677–2068)3745 (3341–4035)5439 (4935–5983)7198 (6579–7871)9055 (8196–9837)10 767 (9882–11 675)
 75% of IL facilities10 (8–13)1991 (1899–2134)3855 (3650–4190)5761 (5455–6145)7623 (7244–8031)9530 (8972–9826)11 372 (10 806–11 763)
 50% of IL facilities11 (9–14)2005 (1845–2125)3951 (3634–4101)5775 (5277–6127)7639 (6912–8171)9532 (8738–10 251)11 383 (10 422–12 273)
 25% of IL facilities10 (8–13)1974 (1869–2153)3948 (3624–4154)5904 (5428–6245)7795 (7254–8275)9771 (9095–10 348)11 652 (10 930–12 269)
Registry ParticipationTime, mo
061218243036
40% of CRE carriers in the XDRO registry, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities11 (9–14)2008 (1816–2153)3877 (3609–4145)5835 (5467–6187)7710 (7298–8131)9585 (9107–10 088)11 532 (10 970–12 152)
 75% of IL facilities10 (8–13)2013 (1854–2114)3919 (3669–4129)5838 (5429–6176)7794 (7292–8361)9678 (9072–10 599)11 637 (10 972–12 805)
 50% of IL facilities12 (10–15)1980 (1911–2147)3969 (3770–4202)5926 (5574–6303)7855 (7448–8467)9943 (9299–10 665)11 955 (11 141–12 912)
 25% of IL facilities11 (9–14)2002 (1847–2170)3987 (3701–4210)5893 (5510–6409)7761 (7339–8514)9731 (9217–10 583)11 806 (11 211–12 673)
80% of CRE carriers in the XDRO registry, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities11 (8–14)1905 (1677–2068)3745 (3341–4035)5439 (4935–5983)7198 (6579–7871)9055 (8196–9837)10 767 (9882–11 675)
 75% of IL facilities10 (8–13)1991 (1899–2134)3855 (3650–4190)5761 (5455–6145)7623 (7244–8031)9530 (8972–9826)11 372 (10 806–11 763)
 50% of IL facilities11 (9–14)2005 (1845–2125)3951 (3634–4101)5775 (5277–6127)7639 (6912–8171)9532 (8738–10 251)11 383 (10 422–12 273)
 25% of IL facilities10 (8–13)1974 (1869–2153)3948 (3624–4154)5904 (5428–6245)7795 (7254–8275)9771 (9095–10 348)11 652 (10 930–12 269)

Only facilities in the Chicago region within the state of Illinois were eligible to participate in the XDRO registry—100% of eligible facilities: 402 facilities and 64 022 total beds; 75% of eligible facilities: 304 facilities and 57 022 beds (89% of total eligible); 50% of eligible facilities: 201 facilities and 44 382 beds (69% of total eligible); 25% of eligible facilities: 101 facilities and 27 232 beds (43% of total eligible).

Abbreviations: CRE, carbapenem-resistant Enterobacteriaceae; IL, Illinois; IQR, interquartile range; XDRO, extensively drug-resistant organism.

Table 2.

Cumulative Number of Incident Carbapenem-resistant Enterobacteriaceae (CRE) Carriers Regionwide at Given Points in Time With and Without the Use of an Extensively Drug-resistant Organism (XDRO) Registry, Varying the Percentage of CRE Carriers Identified With Registry Use, in Various Groupings of Healthcare Facilities

Registry ParticipationTime, mo
061218243036
40% of CRE carriers in the XDRO registry, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities11 (9–14)2008 (1816–2153)3877 (3609–4145)5835 (5467–6187)7710 (7298–8131)9585 (9107–10 088)11 532 (10 970–12 152)
 75% of IL facilities10 (8–13)2013 (1854–2114)3919 (3669–4129)5838 (5429–6176)7794 (7292–8361)9678 (9072–10 599)11 637 (10 972–12 805)
 50% of IL facilities12 (10–15)1980 (1911–2147)3969 (3770–4202)5926 (5574–6303)7855 (7448–8467)9943 (9299–10 665)11 955 (11 141–12 912)
 25% of IL facilities11 (9–14)2002 (1847–2170)3987 (3701–4210)5893 (5510–6409)7761 (7339–8514)9731 (9217–10 583)11 806 (11 211–12 673)
80% of CRE carriers in the XDRO registry, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities11 (8–14)1905 (1677–2068)3745 (3341–4035)5439 (4935–5983)7198 (6579–7871)9055 (8196–9837)10 767 (9882–11 675)
 75% of IL facilities10 (8–13)1991 (1899–2134)3855 (3650–4190)5761 (5455–6145)7623 (7244–8031)9530 (8972–9826)11 372 (10 806–11 763)
 50% of IL facilities11 (9–14)2005 (1845–2125)3951 (3634–4101)5775 (5277–6127)7639 (6912–8171)9532 (8738–10 251)11 383 (10 422–12 273)
 25% of IL facilities10 (8–13)1974 (1869–2153)3948 (3624–4154)5904 (5428–6245)7795 (7254–8275)9771 (9095–10 348)11 652 (10 930–12 269)
Registry ParticipationTime, mo
061218243036
40% of CRE carriers in the XDRO registry, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities11 (9–14)2008 (1816–2153)3877 (3609–4145)5835 (5467–6187)7710 (7298–8131)9585 (9107–10 088)11 532 (10 970–12 152)
 75% of IL facilities10 (8–13)2013 (1854–2114)3919 (3669–4129)5838 (5429–6176)7794 (7292–8361)9678 (9072–10 599)11 637 (10 972–12 805)
 50% of IL facilities12 (10–15)1980 (1911–2147)3969 (3770–4202)5926 (5574–6303)7855 (7448–8467)9943 (9299–10 665)11 955 (11 141–12 912)
 25% of IL facilities11 (9–14)2002 (1847–2170)3987 (3701–4210)5893 (5510–6409)7761 (7339–8514)9731 (9217–10 583)11 806 (11 211–12 673)
80% of CRE carriers in the XDRO registry, median (IQR)
 No XDRO registry11 (10–14)2098 (1985–2234)4178 (3970–4461)6316 (5976–6618)8493 (7872–8962)10 615 (9854–11 243)12 735 (12 012–13 579)
 100% of IL facilities11 (8–14)1905 (1677–2068)3745 (3341–4035)5439 (4935–5983)7198 (6579–7871)9055 (8196–9837)10 767 (9882–11 675)
 75% of IL facilities10 (8–13)1991 (1899–2134)3855 (3650–4190)5761 (5455–6145)7623 (7244–8031)9530 (8972–9826)11 372 (10 806–11 763)
 50% of IL facilities11 (9–14)2005 (1845–2125)3951 (3634–4101)5775 (5277–6127)7639 (6912–8171)9532 (8738–10 251)11 383 (10 422–12 273)
 25% of IL facilities10 (8–13)1974 (1869–2153)3948 (3624–4154)5904 (5428–6245)7795 (7254–8275)9771 (9095–10 348)11 652 (10 930–12 269)

Only facilities in the Chicago region within the state of Illinois were eligible to participate in the XDRO registry—100% of eligible facilities: 402 facilities and 64 022 total beds; 75% of eligible facilities: 304 facilities and 57 022 beds (89% of total eligible); 50% of eligible facilities: 201 facilities and 44 382 beds (69% of total eligible); 25% of eligible facilities: 101 facilities and 27 232 beds (43% of total eligible).

Abbreviations: CRE, carbapenem-resistant Enterobacteriaceae; IL, Illinois; IQR, interquartile range; XDRO, extensively drug-resistant organism.

Seventy-five Percent of State Healthcare Facilities Participating and Utilizing the XDRO Registry

When 75% of the largest Illinois facilities by bed size used a registry (n = 304: 68 hospitals, 2 LTACHs, 9 vSNFs, 225 SNFs; 57 022 beds), prevalence in healthcare facilities regionwide dropped by a relative 5.0% (compared to no registry) after 3 years to 1.46% (Figure 1). Registry use resulted in an additional 35 625 contact precaution days per year and averted 1473 incident CRE carriers in 3 years (11.6% relative reduction; Table 1). As Figure 2 shows, while the effects were similar to when 100% of Illinois facilities participated in a registry, 100% participation may yield additional gains. Hospitals experienced the largest relative reductions in carriers (14.2%), followed by vSNFs (10.2%) and LTACHs (4.6%); again, SNFs had no change. Those in-state facilities using the registry had a 16.9% relative reduction in new carriers (6776 vs 8155) over the 3-year period compared to when these same facilities were not using the registry (Figure 3) and a 5.9% relative decrease in prevalence at year 3. Those not participating had a 1.2% relative decrease (4584 vs 4638) in new carriers over 3 years (Figure 3) and a 3.2% relative decrease in prevalence at year 3, showing that indirect effects were small but detectable.

Registry use resulted in a 4.2% and 6.8% relative reduction in prevalence regionwide when 40% and 80% of all carriers were in the registry, respectively. Table 2 shows the number of new carriers over time.

Fifty Percent of State Healthcare Facilities Participating and Utilizing the XDRO Registry

CRE prevalence in healthcare facilities regionwide at year 3 dropped by a relative 5.6% when 50% of the largest facilities in Illinois used a registry (n = 201: 55 hospitals, 8 vSNFs, 138 SNFs; 44 382 beds). Registry use resulted in 22 485 additional contact precaution days per year, averting 1358 new carriers over the 3-year period (10.7% relative reduction; Table 1). Overall, the gains achieved when 50% participated were enough that little was garnered when increasing to 75% facility participation (Figure 2). Again, hospitals and vSNFs garnered the greatest benefits. The registry had direct and indirect impacts with a 21.9% and 2.3% relative reduction in total incident CRE carriers in participating and nonparticipating facilities, respectively, compared to no registry (Figure 3).

Registry use decreased the number of new carriers by a relative 6.1% (780 fewer) regionwide when only 40% of all carriers were in the registry and by a relative 10.6% (1352 fewer) when 80% of carriers were in the registry (Table 2).

Twenty-five Percent of State Healthcare Facilities Participating and Utilizing the XDRO Registry

Regionwide CRE prevalence at year 3 dropped by a relative 2.8% when 25% of the largest facilities in Illinois used a registry (n = 101: 38 hospitals, 6 vSNFs, 57 SNFs; 27 232 beds). Registry use resulted in 21 619 additional contact precaution days each year, averting 1165 incident carriers over 3 years regionwide (9.1% relative reduction; Table 1). As Figure 2 shows, benefits are garnered regionwide even when only 25% of the largest facilities participate compared to no registry. Hospitals and vSNFs achieved the greatest relative reductions in new carriers (11.6% and 6.8%, respectively) over the 3-year period. Compared to not using a registry, an XDRO registry resulted in a 20.4% relative reduction in total incident carriers in participating facilities and a 1.6% relative reduction in nonparticipating facilities over a 3-year period (Figure 3).

When 40% of carriers are in the XDRO registry, its use averted 929 new carriers regionwide after 3 years (7.3% relative decrease; Table 2). When 80% of all carriers are in the registry, its use resulted in a 4.8% and 8.5% relative reduction in CRE prevalence and new carriers, respectively.

DISCUSSION

Implementing a regionwide electronic public health registry can reduce CRE’s spread in the region (up to 15.5% relative reduction in incident carriers over 3 years). Even limited deployment of an XDRO registry (eg, 25% of largest facilities; 101 of 402) had an impact on the number of new carriers regionwide. There is value even when 25% of facilities participate as the registry captures a sufficient amount of CRE carriers (which are identified and placed on contact precautions) to substantially dampen transmission. While increasing deployment increased gains, additional benefits accumulate more slowly as more and more facilities participate (when deploying by bed size). In fact, the largest gains were garnered when going from 0% to 25% of the largest facilities participating in a registry (which represented 43% of beds in the Chicago region within Illinois). Additionally, even when only 40% of all carriers are in the registry, its use reduced CRE prevalence and transmission regionwide. Overall, hospitals garnered the largest reductions as more utilize the registry and hospital beds make up the largest fraction of total beds in Illinois that would identify more carriers with a registry (26% of total); followed by vSNFs and LTACHs, which have a higher overall and admission CRE prevalence, longer LOSs, and generally higher transmission coefficients. Facilities that did not participate also experienced a decrease in CRE over time, albeit at a lower rate compared to participants, showing that deployment of a public health registry has important benefits for participants and nonparticipants, even those in neighboring states.

Public health surveillance of a disease is traditionally viewed as the first step of disease prevention; the data obtained from surveillance and its dissemination allow for focusing public health action on prevention. The electronic public health registry is unique in that it serves as a surveillance system that by itself can prevent infection by transmitting actionable data directly to healthcare providers. Our modeling suggests that a surveillance system has the potential for disease prevention, independent of downstream public health efforts that implement additional prevention measures.

Our results show that an XDRO registry may be an effective tool in combating XRDO spread between facilities in a region. Appropriately identifying patients allows for prompt use of contact precautions, which may save resources and time if known carriers do not need to be reidentified. However, as CRE reductions were modest, other infection prevention and control measures should be used in conjunction with a registry. For example, in the absence of routine screening, only a fraction of CRE carriers may actually be identified and added to the registry. Admission screening of patients directly transferred to hospitals and LTACHs and contact isolation of CRE-positive patients can reduce CRE’s burden [14]. Thus, admission screening to identify additional carriers could potentially enhance the benefits of a registry as more carriers are identified. However, there is a trade-off between identifying more carriers and resource use (eg, screening materials, isolation capacity). Compared to other CRE prevention and control measures, an XDRO registry may perform better than ring surveillance at preventing transmission events [19], but may not be as effective as regional and national active screening interventions [14, 15, 20], or a bundled intervention that includes chlorhexidine gluconate bathing and cohorting [21].

Our study may actually underestimate the value of an XDRO registry, depending on the circumstances. For example, if the prevalence of CRE were lower and limited to only some facilities, a registry could help identify cases before CRE could spread, reach other facilities, and become more established in a region, thus preventing many more cases. Such a registry could help prevent and control the spread of other antibiotic resistant organisms as well (eg, by capturing other pathogens [2] or identifying co-colonized patients). Currently, there is a dearth of registry evaluations. This modeling study represents one of the initial assessments and demonstrates that it takes time to garner reductions in CRE transmission and prevalence and comprehensively capture a registry’s value. Future studies can determine the value of registries currently implemented.

There are limitations to this study. All models are simplifications of real life [22] and thus cannot represent every event or outcome. While our model is populated with data from one region, we include several different types of healthcare facilities, across a diverse population, and wide geographic area. Results may be different in different parts of the country if patient sharing is uncommon due to geographic distances or insurance restrictions. We are limited to Centers for Medicare and Medicaid Services patient data, which may not represent the transfer patterns of all patients as these patients tend to be older and present with more comorbidities. Our model assumes minimal community CRE transmission and does not explicitly represent potential transmission in the community or other settings. We assumed compliance with contact precautions was consistent over time. However, compliance could decline as more patients are placed on precautions [23], and the reported effectiveness of gloves and gowns to reduce extended-spectrum β-lactamase transmission varies [24, 25]. Additionally, we did not distinguish between CRE colonization and infection, as we intended to evaluate registry use for any CRE carrier.

CONCLUSIONS

Implementing a regionwide XDRO registry could reduce CRE’s spread in a region (up to 15.5% relative reduction in new carriers over 3 years). Benefits accrue even with modest participation by facilities, benefiting both participants and nonparticipants. We found that a registry can provide independent effects of disease prevention, even before additional public health prevention measures are implemented.

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

Disclaimer. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript.

Financial support. This work was supported by the Agency for Healthcare Research and Quality (grant number R01HS023317); the Centers for Disease Control and Prevention (SHEPheRD contract number 200-2011-42037 and Prevention Epicenter cooperative agreement number U54CK000481); the Eunice Kennedy Shriver National Institute of Child Health and Human Development (grant number U01HD086861), the Office of Behavioral and Social Sciences Research, and the Global Obesity Prevention Center (grant number U54HD070725).

Potential conflicts of interest. M. K. H. has been a coinvestigator on research studies that received support in the form of contributed product from Clorox, Medline, Mölnlycke, OpGen, and Sage Products, and has received an investigator-initiated grant from Clorox. R. A. W. has been a coinvestigator on research studies that received support in the form of contributed product from Clorox, Mölnlycke, Medline, and Sage Products. W. E. T. has research support from the Washington Square Foundation and CareFusion Foundation. M. Y. L. has received research support in the form of contributed product from OpGen and Sage Products (now part of Stryker Corporation) and has received an investigator-initiated grant from CareFusion Foundation (now part of BD). All other authors report no potential conflicts of interest. 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.

References

1.

Trick
WE
,
Lin
MY
,
Cheng-Leidig
R
, et al.
Electronic public health registry of extensively drug-resistant organisms, Illinois, USA
.
Emerg Infect Dis
2015
;
21
:
1725
32
.

2.

Kho
AN
,
Doebbeling
BN
,
Cashy
JP
, et al.
A regional informatics platform for coordinated antibiotic-resistant infection tracking, alerting, and prevention
.
Clin Infect Dis
2013
;
57
:
254
62
.

3.

Pfeiffer
CD
,
Cunningham
MC
,
Poissant
T
, et al.
Establishment of a statewide network for carbapenem-resistant Enterobacteriaceae prevention in a low-incidence region
.
Infect Control Hosp Epidemiol
2014
;
35
:
356
61
.

4.

Centers for Disease Control and Prevention, National Center for Emerging and Zoonotic Infectious Diseases, Division of Healthcare Quality Promotion
.
Antibiotic/antimicrobial resistance. Biggest threats
. Available at: https://www.cdc.gov/drugresistance/biggest_threats.html. Accessed
5 May 2018
.

5.

Bartsch
SM
,
McKinnell
JA
,
Mueller
LE
, et al.
Potential economic burden of carbapenem-resistant Enterobacteriaceae (CRE) in the United States
.
Clin Microbiol Infect
2017
;
23
:
48.e9
16
.

6.

Falagas
ME
,
Tansarli
GS
,
Karageorgopoulos
DE
,
Vardakas
KZ
.
Deaths attributable to carbapenem-resistant Enterobacteriaceae infections
.
Emerg Infect Dis
2014
;
20
:
1170
5
.

7.

Ventola
CL
.
The antibiotic resistance crisis: part 1: causes and threats
.
P T
2015
;
40
:
277
83
.

8.

Gandra
S
,
Barter
DM
,
Laxminarayan
R
.
Economic burden of antibiotic resistance: how much do we really know?
Clin Microbiol Infect
2014
;
20
:
973
80
.

9.

Lee
BY
,
McGlone
SM
,
Song
Y
, et al.
Social network analysis of patient sharing among hospitals in Orange County, California
.
Am J Public Health
2011
;
101
:
707
13
.

10.

Lee
BY
,
Song
Y
,
Bartsch
SM
, et al.
Long-term care facilities: important participants of the acute care facility social network?
PLoS One
2011
;
6
:
e29342
.

11.

Lee
BY
,
McGlone
SM
,
Wong
KF
, et al.
Modeling the spread of methicillin-resistant Staphylococcus aureus (MRSA) outbreaks throughout the hospitals in Orange County, California
.
Infect Control Hosp Epidemiol
2011
;
32
:
562
72
.

12.

Lee
BY
,
Yilmaz
SL
,
Wong
KF
, et al.
Modeling the regional spread and control of vancomycin-resistant enterococci
.
Am J Infect Control
2013
;
41
:
668
73
.

13.

Lee
BY
,
Bartsch
SM
,
Wong
KF
, et al.
The importance of nursing homes in the spread of methicillin-resistant Staphylococcus aureus (MRSA) among hospitals
.
Med Care
2013
;
51
:
205
15
.

14.

Lee
BY
,
Bartsch
SM
,
Wong
KF
, et al.
The potential trajectory of carbapenem-resistant Enterobacteriaceae, an emerging threat to health-care facilities, and the impact of the Centers For Disease Control and Prevention toolkit
.
Am J Epidemiol
2016
;
183
:
471
9
.

15.

Slayton
RB
,
Toth
D
,
Lee
BY
, et al.
Vital signs: estimated effects of a coordinated approach for action to reduce antibiotic-resistant infections in health care facilities—United States
.
MMWR Morb Mortal Wkly Rep
2015
;
64
:
826
31
.

16.

Ray
MJ
,
Lin
MY
,
Weinstein
RA
,
Trick
WE
.
Spread of carbapenem-resistant Enterobacteriaceae among Illinois healthcare facilities: the role of patient sharing
.
Clin Infect Dis
2016
;
63
:
889
93
.

17.

Lee
BY
,
Wong
KF
,
Bartsch
SM
, et al.
The Regional Healthcare Ecosystem Analyst (RHEA): a simulation modeling tool to assist infectious disease control in a health system
.
J Am Med Inform Assoc
2013
;
20
:
e139
46
.

18.

Prabaker
K
,
Lin
MY
,
McNally
M
, et al.
Centers for Disease Control and Prevention (CDC) Prevention Epicenters Program
.
Transfer from high-acuity long-term care facilities is associated with carriage of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae: a multihospital study
.
Infect Control Hosp Epidemiol
2012
;
33
:
1193
9
.

19.

Fitzpatrick
M
,
Zembower
T
,
Malczynski
M
,
Qi
C
,
Bolon
MK
.
Outcomes of an enhanced surveillance program for carbapenem-resistant Enterobacteriaceae
.
Infect Control Hosp Epidemiol
2014
;
35
:
419
22
.

20.

Schwaber
MJ
,
Carmeli
Y
.
An ongoing national intervention to contain the spread of carbapenem-resistant Enterobacteriaceae
.
Clin Infect Dis
2014
;
58
:
697
703
.

21.

Hayden
MK
,
Lin
MY
,
Lolans
K
, et al.
Centers for Disease Control and Prevention Epicenters Program
.
Prevention of colonization and infection by Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae in long-term acute-care hospitals
.
Clin Infect Dis
2015
;
60
:
1153
61
.

22.

Lee
BY
.
Digital decision making: computer models and antibiotic prescribing in the twenty-first century
.
Clin Infect Dis
2008
;
46
:
1139
41
.

23.

Dhar
S
,
Marchaim
D
,
Tansek
R
, et al.
Contact precautions: more is not necessarily better
.
Infect Control Hosp Epidemiol
2014
;
35
:
213
21
.

24.

Tschudin-Sutter
S
,
Lucet
JC
,
Mutters
NT
,
Tacconelli
E
,
Zahar
JR
,
Harbarth
S
.
Contact precautions for preventing nosocomial transmission of extended-spectrum β lactamase-producing Escherichia coli: a point/counterpoint review
.
Clin Infect Dis
2017
;
65
:
342
7
.

25.

Zahar
JR
,
Blot
S
,
Nordmann
P
, et al.
Screening for intestinal carriage of ESBL-producing Enterobacteriaceae in critically ill patients: expected benefits and evidence-based controversies [manuscript published online ahead of print 12 October 2018]
.
Clin Infect Dis
2018
. doi:10.1093/cid/ciy864.

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