infection control & hospital epidemiology
october 2015, vol. 36, no. 10
original article
Prevalence of and Risk Factors for Multidrug-Resistant Acinetobacter baumannii Colonization Among High-Risk Nursing Home Residents Lona Mody, MD, MSc;1,2 Kristen E. Gibson, MPH;1 Amanda Horcher, MPH;3 Katherine Prenovost, PhD;4 Sara E. McNamara, MPH, MT(ASCP);1 Betsy Foxman, PhD;3 Keith S. Kaye, MD, MPH;5 Suzanne Bradley, MD;6 on behalf of the Targeted Infection Prevention Study Team, Ann Arbor, Michigan
objective. To characterize the epidemiology of multidrug-resistant (MDR) Acinetobacter baumannii colonization in high-risk nursing home (NH) residents. design. setting.
Nested case-control study within a multicenter prospective intervention trial. Four NHs in Southeast Michigan.
participants. Case patients and control subjects were NH residents with an indwelling device (urinary catheter and/or feeding tube) selected from the control arm of the Targeted Infection Prevention study. Cases were residents colonized with MDR (resistant to ≥3 classes of antibiotics) A. baumannii; controls were never colonized with MDR A. baumannii. methods. For active surveillance cultures, specimens from the nares, oropharynx, groin, perianal area, wounds, and device insertion site(s) were collected upon study enrollment, day 14, and monthly thereafter. A. baumannii strains and their susceptibilities were identified using standard microbiologic methods. results. Of 168 NH residents, 25 (15%) were colonized with MDR A. baumannii. Compared with the 143 controls, cases were more functionally disabled (Physical Self-Maintenance Score >24; odds ratio, 5.1 [95% CI, 1.8–14.9]; P < .004), colonized with Proteus mirabilis (5.8 [1.9–17.9]; P < .003), and diabetic (3.4 [1.2–9.9]; P < .03). Most cases (22 [88%]) were colonized with multiple antibiotic-resistant organisms and 16 (64%) exhibited co-colonization with at least one other resistant gram-negative bacteria. conclusion. Functional disability, P. mirabilis colonization, and diabetes mellitus are important risk factors for colonization with MDR A. baumannii in high-risk NH residents. A. baumannii exhibits widespread antibiotic resistance and a preference to colonize with other antibiotic-resistant organisms, meriting enhanced attention and improved infection control practices in these residents. Infect. Control Hosp. Epidemiol. 2 01 5 ;3 6 (1 0) :1 15 5 – 11 62
Acinetobacter baumannii is a gram-negative bacterium that causes a wide range of monomicrobial and polymicrobial infections, including bacteremia, pneumonia, urinary tract infections, deep wound infections, and osteomyelitis.1–5 One of the largest challenges in treating A. baumannii infections is the organism’s capacity to rapidly acquire antibiotic resistance.1–3,6–12 Pan-resistant A. baumannii isolates have emerged, including isolates resistant to carbapenems, colistin, and polymyxins, rendering these strains virtually untreatable.1,3,6,8,9,12–17 Certain strains of A. baumannii have the ability to form biofilms and persist in the environment,18–20 including on
horizontal surfaces and medical devices such as urinary catheters and intravenous lines, facilitating the organism’s spread from patient to patient via the hands of healthcare workers.10–21 Resistance to disinfectants further contributes to the persistence of the A. baumannii in the environment and the development of endemics and epidemics in long-term and acute care facilities, sometimes requiring the closure of entire wings to contain the outbreaks and stop spread.1,3,6,8,12,15,22,23 Multidrug-resistant (MDR) A. baumannii were initially confined to acute care hospitals. Recently, MDR A. baumannii has been reported to cause infection among hospitalized older adults in long-term care settings, especially in those with
Affiliations: 1. Division of Geriatric and Palliative Care Medicine, University of Michigan Medical School, Ann Arbor, Michigan; 2. Geriatrics Research Education and Clinical Center, Veterans Affairs Ann Arbor Healthcare System, Ann Arbor, Michigan; 3. Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, Michigan; 4. Veterans Affairs Center for Clinical Management Research, Ann Arbor, Michigan; 5. Division of Infectious Diseases, Detroit Medical Center and Wayne State University, Detroit, Michigan; 6. Infectious Diseases Section, Veterans Affairs Ann Arbor Healthcare System and the University of Michigan Medical School, Ann Arbor, Michigan. Received March 6, 2015; accepted May 6, 2015; electronically published June 15, 2015 © 2015 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2015/3610-0005. DOI: 10.1017/ice.2015.143
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october 2015, vol. 36, no. 10
invasive devices and/or underlying comorbidities.9,14–15,22,24–28 Nursing home (NH) residents have many of the risk factors that may contribute to colonization or infection with MDR A. baumannii, including chronic obstructive pulmonary disorder, cardiac and renal failure, diabetes mellitus, dementia, presence of wounds, and use of antibiotics and invasive devices such as urinary catheters.3,6,12,14,15,22,29–31 Although recent studies emphasize the emerging role of NHs in the acquisition and transmission of MDR A. baumannii,24–26 few studies focus on NH residents within the long-term care environment. Our study begins to fill this gap by characterizing the clinical and microbiologic epidemiology of MDR A. baumannii colonization in NH residents. We were particularly interested in the role of functional disability and age-related comorbidities in predicting A. baumannii colonization. We also explored the association of co-colonization with other antibiotic-resistant organisms (AROs), including methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), and resistant gram-negative bacteria (R-GNB) in predicting A. baumannii colonization.
m e th o d s Study Population and Design The goal of the larger, cluster-randomized intervention trial was to design, implement, and evaluate the efficacy of a multicomponent Targeted Infection Prevention (TIP) program in reducing MDR organism (MDRO) prevalence and infections in a high-risk NH population.32 The TIP study was approved by the University of Michigan Institutional Review Board and was conducted in 12 (6 control, 6 intervention) community-based NHs in Michigan.33 Study inclusion criteria were (a) any short- or long-stay resident with an indwelling urinary catheter (urethral or suprapubic) and/or a feeding tube (nasogastric or percutaneous endoscopic gastrostomy tube) for more than 72 hours (residents with long-standing devices as well as new devices were included since all residents with devices were at risk for new MDRO acquisition or infection), and (b) provision of informed consent. Residents receiving end-of-life care were excluded. Specimens were collected from enrolled residents at the time of enrollment, on day 14, and monthly thereafter for a maximum of 1 year (or until death, discharge, or device discontinuation) for outcome measurements. Residents who were admitted to acute care hospitals and returned to the NH remained in the study. Clinical and demographic data on the participants were obtained from the source documents at the participating facility and medical chart review conducted by trained research staff. Using participants from the 6 control NHs, we conducted a nested case-control study to evaluate predictors related to colonization with MDR A. baumannii. Participants in intervention NHs were excluded to avoid any influence due to intervention effects.
Case and Control Definitions We defined case patients as residents with indwelling devices and laboratory-confirmed A. baumannii colonization with resistance to at least 3 classes of antibiotics at any point during their participation in the TIP study. Control subjects were defined as residents with indwelling devices without MDR A. baumannii colonization at any point during the TIP study and came only from facilities with cases. Data Collection Demographic characteristics, comorbidities, Physical SelfMaintenance Score (PSMS) for functional status assessment, device use, and prior antibiotic use were obtained from medical records at baseline, day 14, and monthly thereafter. Demographic information collected included age, sex, baseline weight, race, ethnicity, frequency of family visits, advance directive code, falls in the past 30 days, hospitalization in the past 30 days, presence of wounds, presence of pressure sores, and history of MDROs. Comorbidities gathered were based on the Charlson comorbidity index.34 Lawton and Brody’s PSMS was used to measure functional disability (scale from 6 to 30, with increasing scores indicating increasing disability).35 Device use was recorded as a resident having either a urinary catheter or feeding tube or both. If the device was removed at any point during follow-up, the resident was discharged from the study. Any new infections during follow-up, regardless of case status, were recorded. Additionally, the use of antibiotics to treat any infection, including the type of antibiotic and duration of use, was recorded. Microbiological Methods Active surveillance cultures for MDROs from multiple anatomic sites were performed at regular intervals by obtaining microbiologic samples from resident nares, oropharynx, enteral feeding tube and suprapubic device insertion sites, groin, perianal area, and wounds at baseline, day 14, and then monthly for up to 1 year, regardless of prior colonization status. Standard microbiologic methods were used to identify MRSA, VRE, ceftazidime-resistant gram-negative bacilli, and ciprofloxacin-resistant gram-negative bacilli as previously described.36 If more than one organism was identified from a sample, that resident was deemed to be co-colonized at that specific body site. A. baumannii were initially identified by API20E (Oxoid) and screened for resistance to either ceftazidime or ciprofloxacin using standard disc diffusion methods.14 All presumptive A. baumannii isolates were confirmed to the species level by the University of Michigan Clinical Microbiology Laboratory using matrix-assisted laser desorption ionization-time of flight mass spectrometry (Biotyper RUO; Bruker).37 Antimicrobial susceptibilities were verified by Vitek 2 using the GN82 AST (bioMérieux), according to Clinical
acinetobacter baumannii in nursing homes
and Laboratory Standards Institutes criteria and defined breakpoints.38 Tested antibiotic classes included (1) penicillin combinations (ampicillin/sulbactam and piperacillin/tazobactam); (2) aztreonam; (3) first-, third-, and fourthgeneration cephalosporins; (4) aminoglycosides (gentamicin and tobramycin); (5) quinolones (ciprofloxacin and levofloxacin); (6) carbapenems (imipenem and meropenem); (7) tetracycline; and (8) trimethoprim/sulfamethoxazole. Topical and antiseptic agents were not included in antimicrobial profiles. A. baumannii strains resistant to 3 or more classes of antibiotics were considered MDR.29 Statistical Analyses Data were entered into a master database (Access 2007; Microsoft) and analyzed using Stata, version 13.1 (StataCorp). The associations of key predictors with MDR A. baumannii colonization were examined using exact logistic regression adjusting for NH site to appropriately account for nesting and small sample sizes. Clustered logistic regression was used with exact logistic regression models for 2 reasons: (1) the clustered element was to account for the dependencies in the outcomes by facility, and (2) the exact logistic framework was used to address parameter estimation for small sample sizes. To explore more-complex associations among several predictors and MDR A. baumannii colonization, all prior statistically significant variables that had enough data were included in an augmented logistic model. The multivariable model was empirically driven on the basis of results from the previously run bivariate models using alpha ≤ .05.
results Study Population In the 6 control NHs, 215 residents or their legal guardian provided consent and were enrolled in the TIP study. No cases of MDR A. baumannii colonization occurred in 2 facilities, thus controls from these 2 NHs were excluded from further analysis (n = 47). The number of cases at the 4 remaining facilities varied, with facility E contributing the most (12 [48% of cases]) and facility G contributing the fewest (1 [4% of cases]). Facilities also differed in the degree of short- vs longterm care; the median length of stay among enrolled residents at facility K was 170 days compared with other facilities with median stays less than 90 days. Of the 168 residents with an indwelling device at 4 facilities, 25 (15%) were colonized at least once with MDR A. baumannii, all of which were resistant to cephalosporins, monobactam (aztreonam), and quinolones. Twenty-four cases (96%) carried A. baumannii resistant to 9 or more commonly used antibiotics. Most cases (20 [80%]) were colonized with carbapenem-resistant A. baumannii, accounting for 68.9% of isolates (93/135). Of the 25 cases, 16 (64%) were preexisting, or present on study enrollment, whereas 9 (36%) were new acquisitions. Eleven cases
1157
(44%) involved recurrent A. baumannii colonization and 14 (56%) were colonized on a single visit (Figure 1). Cases and controls were similar in baseline characteristics including age, sex, comorbidity score, rate of recent hospitalizations and antibiotic use, number of antibiotic classes used, and proportion of patients with urinary catheters (Table 1). Cases differed from controls in terms of functional disability, length of stay, total follow-up time, and presence of multiple indwelling devices. Cases had greater mean (SD) functional disability on average than controls (24.0 [3.8] vs 20.9 [4.5]), longer mean stays in the NH facility before enrollment (657 vs 133 days), and longer mean follow-up (151 vs 55 days). Risk Factors for MDR A. baumannii Colonization Clustered exact logistic regression models showed that colonization with MDR A. baumannii was significantly associated with functional disability. A high level of disability (PSMS score >24) was associated with a 4.3 times greater likelihood of MDR A. baumannii colonization (95% CI, 1.5–12.8; P < .006). Residents with both a feeding tube and urinary catheter were approximately 6 times more likely than residents with only one device to have MDR A. baumannii colonization (odds ratio, 6.1 [95% CI, 1.8–21.1]; P < .003). Diabetes was marginally associated with A. baumannii colonization (odds ratio, 2.9 [95% CI, 1.0–8.6]; P < .05). Co-colonization With Other AROs We evaluated the frequency of colonization with R-GNB, MRSA, and VRE prior to or concurrent with the first incidence of a positive MDR A. baumannii culture (Table 2). Of the 25 cases, 22 (88%) had at least one incidence of ARO colonization; Proteus mirabilis was the most prevalent organism among cases (56%), followed by VRE (48%), MRSA (44%), and Escherichia coli (44%). Of the 143 controls, 100 (70%) were colonized with at least one ARO during study follow-up; MRSA was the most prevalent organism among controls (43%), followed by VRE (25%), E. coli (23%), and P. mirabilis (17%). We were also interested in the frequency of co-colonization (ie, colonizing the same body site on the same visit) between MDR A. baumannii and other R-GNBs. Sixteen cases (64%) were considered to be co-colonized. Of 48 swab samples that indicated co-colonization, 30 (63%) revealed a single co-colonizing organism (in addition to A. baumannii) and 17 (35%) revealed 2 co-colonizing organisms. In one swab sample, MDR A. baumannii and antibiotic-resistant P. mirabilis, E. coli, and Morganella morgannii were all isolated from the perianal area of one resident. Table 3 describes the frequency of co-colonizing organisms isolated from 4 different body sites. Multivariable Model Examining A. baumannii Colonization We explored the association among several predictors that were significant in bivariate models and MDR A. baumannii
1158 infection control & hospital epidemiology
october 2015, vol. 36, no. 10
figure 1. Temporal trends of multidrug-resistant (MDR) Acinetobacter baumannii acquisition. Each row corresponds to a different nursing home resident and each column represents a follow-up visit. The mean length of stay prior to visit 0 among these residents was 657 days. White squares correspond to a follow-up day during which residents were not colonized with MDR A. baumannii; gray squares correspond to days in which swab specimens were not collected or days for which that resident was lost to follow-up. An X represents MDR A. baumannii colonization; an asterisk indicates recurrent MDR A. baumannii colonization.
table 1. Controls
Demographic Characteristics of Cases (With Multidrug-Resistant Acinetobacter baumannii Colonization) and
Characteristic Age, mean (SD), years Male sex History of MRSA History of VRE PSMS score, mean (SD) Comorbidity score, mean (SD) Device type at baseline Urinary catheter (UC) only Feeding tube (FT) only Both UC and FT Antibiotic usage within 30 daysa No. antibiotic classes used, mean (SD)b Hospitalization within 30 days Length of stay, mean, daysc Total follow-up, mean, daysd
Cases (n = 25)
Controls (n = 143)
P
68 (14) 16 (64) 7 (28) 1 (4) 24.0 (3.8) 3.7 (2.1)
70 (13) 83 (58) 25 (17) 14 (10) 20.9 (4.5) 3.0 (2.4)
.44 .58 .05 .68
october 2015, vol. 36, no. 10
original article
Prevalence of and Risk Factors for Multidrug-Resistant Acinetobacter baumannii Colonization Among High-Risk Nursing Home Residents Lona Mody, MD, MSc;1,2 Kristen E. Gibson, MPH;1 Amanda Horcher, MPH;3 Katherine Prenovost, PhD;4 Sara E. McNamara, MPH, MT(ASCP);1 Betsy Foxman, PhD;3 Keith S. Kaye, MD, MPH;5 Suzanne Bradley, MD;6 on behalf of the Targeted Infection Prevention Study Team, Ann Arbor, Michigan
objective. To characterize the epidemiology of multidrug-resistant (MDR) Acinetobacter baumannii colonization in high-risk nursing home (NH) residents. design. setting.
Nested case-control study within a multicenter prospective intervention trial. Four NHs in Southeast Michigan.
participants. Case patients and control subjects were NH residents with an indwelling device (urinary catheter and/or feeding tube) selected from the control arm of the Targeted Infection Prevention study. Cases were residents colonized with MDR (resistant to ≥3 classes of antibiotics) A. baumannii; controls were never colonized with MDR A. baumannii. methods. For active surveillance cultures, specimens from the nares, oropharynx, groin, perianal area, wounds, and device insertion site(s) were collected upon study enrollment, day 14, and monthly thereafter. A. baumannii strains and their susceptibilities were identified using standard microbiologic methods. results. Of 168 NH residents, 25 (15%) were colonized with MDR A. baumannii. Compared with the 143 controls, cases were more functionally disabled (Physical Self-Maintenance Score >24; odds ratio, 5.1 [95% CI, 1.8–14.9]; P < .004), colonized with Proteus mirabilis (5.8 [1.9–17.9]; P < .003), and diabetic (3.4 [1.2–9.9]; P < .03). Most cases (22 [88%]) were colonized with multiple antibiotic-resistant organisms and 16 (64%) exhibited co-colonization with at least one other resistant gram-negative bacteria. conclusion. Functional disability, P. mirabilis colonization, and diabetes mellitus are important risk factors for colonization with MDR A. baumannii in high-risk NH residents. A. baumannii exhibits widespread antibiotic resistance and a preference to colonize with other antibiotic-resistant organisms, meriting enhanced attention and improved infection control practices in these residents. Infect. Control Hosp. Epidemiol. 2 01 5 ;3 6 (1 0) :1 15 5 – 11 62
Acinetobacter baumannii is a gram-negative bacterium that causes a wide range of monomicrobial and polymicrobial infections, including bacteremia, pneumonia, urinary tract infections, deep wound infections, and osteomyelitis.1–5 One of the largest challenges in treating A. baumannii infections is the organism’s capacity to rapidly acquire antibiotic resistance.1–3,6–12 Pan-resistant A. baumannii isolates have emerged, including isolates resistant to carbapenems, colistin, and polymyxins, rendering these strains virtually untreatable.1,3,6,8,9,12–17 Certain strains of A. baumannii have the ability to form biofilms and persist in the environment,18–20 including on
horizontal surfaces and medical devices such as urinary catheters and intravenous lines, facilitating the organism’s spread from patient to patient via the hands of healthcare workers.10–21 Resistance to disinfectants further contributes to the persistence of the A. baumannii in the environment and the development of endemics and epidemics in long-term and acute care facilities, sometimes requiring the closure of entire wings to contain the outbreaks and stop spread.1,3,6,8,12,15,22,23 Multidrug-resistant (MDR) A. baumannii were initially confined to acute care hospitals. Recently, MDR A. baumannii has been reported to cause infection among hospitalized older adults in long-term care settings, especially in those with
Affiliations: 1. Division of Geriatric and Palliative Care Medicine, University of Michigan Medical School, Ann Arbor, Michigan; 2. Geriatrics Research Education and Clinical Center, Veterans Affairs Ann Arbor Healthcare System, Ann Arbor, Michigan; 3. Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, Michigan; 4. Veterans Affairs Center for Clinical Management Research, Ann Arbor, Michigan; 5. Division of Infectious Diseases, Detroit Medical Center and Wayne State University, Detroit, Michigan; 6. Infectious Diseases Section, Veterans Affairs Ann Arbor Healthcare System and the University of Michigan Medical School, Ann Arbor, Michigan. Received March 6, 2015; accepted May 6, 2015; electronically published June 15, 2015 © 2015 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2015/3610-0005. DOI: 10.1017/ice.2015.143
1156
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october 2015, vol. 36, no. 10
invasive devices and/or underlying comorbidities.9,14–15,22,24–28 Nursing home (NH) residents have many of the risk factors that may contribute to colonization or infection with MDR A. baumannii, including chronic obstructive pulmonary disorder, cardiac and renal failure, diabetes mellitus, dementia, presence of wounds, and use of antibiotics and invasive devices such as urinary catheters.3,6,12,14,15,22,29–31 Although recent studies emphasize the emerging role of NHs in the acquisition and transmission of MDR A. baumannii,24–26 few studies focus on NH residents within the long-term care environment. Our study begins to fill this gap by characterizing the clinical and microbiologic epidemiology of MDR A. baumannii colonization in NH residents. We were particularly interested in the role of functional disability and age-related comorbidities in predicting A. baumannii colonization. We also explored the association of co-colonization with other antibiotic-resistant organisms (AROs), including methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), and resistant gram-negative bacteria (R-GNB) in predicting A. baumannii colonization.
m e th o d s Study Population and Design The goal of the larger, cluster-randomized intervention trial was to design, implement, and evaluate the efficacy of a multicomponent Targeted Infection Prevention (TIP) program in reducing MDR organism (MDRO) prevalence and infections in a high-risk NH population.32 The TIP study was approved by the University of Michigan Institutional Review Board and was conducted in 12 (6 control, 6 intervention) community-based NHs in Michigan.33 Study inclusion criteria were (a) any short- or long-stay resident with an indwelling urinary catheter (urethral or suprapubic) and/or a feeding tube (nasogastric or percutaneous endoscopic gastrostomy tube) for more than 72 hours (residents with long-standing devices as well as new devices were included since all residents with devices were at risk for new MDRO acquisition or infection), and (b) provision of informed consent. Residents receiving end-of-life care were excluded. Specimens were collected from enrolled residents at the time of enrollment, on day 14, and monthly thereafter for a maximum of 1 year (or until death, discharge, or device discontinuation) for outcome measurements. Residents who were admitted to acute care hospitals and returned to the NH remained in the study. Clinical and demographic data on the participants were obtained from the source documents at the participating facility and medical chart review conducted by trained research staff. Using participants from the 6 control NHs, we conducted a nested case-control study to evaluate predictors related to colonization with MDR A. baumannii. Participants in intervention NHs were excluded to avoid any influence due to intervention effects.
Case and Control Definitions We defined case patients as residents with indwelling devices and laboratory-confirmed A. baumannii colonization with resistance to at least 3 classes of antibiotics at any point during their participation in the TIP study. Control subjects were defined as residents with indwelling devices without MDR A. baumannii colonization at any point during the TIP study and came only from facilities with cases. Data Collection Demographic characteristics, comorbidities, Physical SelfMaintenance Score (PSMS) for functional status assessment, device use, and prior antibiotic use were obtained from medical records at baseline, day 14, and monthly thereafter. Demographic information collected included age, sex, baseline weight, race, ethnicity, frequency of family visits, advance directive code, falls in the past 30 days, hospitalization in the past 30 days, presence of wounds, presence of pressure sores, and history of MDROs. Comorbidities gathered were based on the Charlson comorbidity index.34 Lawton and Brody’s PSMS was used to measure functional disability (scale from 6 to 30, with increasing scores indicating increasing disability).35 Device use was recorded as a resident having either a urinary catheter or feeding tube or both. If the device was removed at any point during follow-up, the resident was discharged from the study. Any new infections during follow-up, regardless of case status, were recorded. Additionally, the use of antibiotics to treat any infection, including the type of antibiotic and duration of use, was recorded. Microbiological Methods Active surveillance cultures for MDROs from multiple anatomic sites were performed at regular intervals by obtaining microbiologic samples from resident nares, oropharynx, enteral feeding tube and suprapubic device insertion sites, groin, perianal area, and wounds at baseline, day 14, and then monthly for up to 1 year, regardless of prior colonization status. Standard microbiologic methods were used to identify MRSA, VRE, ceftazidime-resistant gram-negative bacilli, and ciprofloxacin-resistant gram-negative bacilli as previously described.36 If more than one organism was identified from a sample, that resident was deemed to be co-colonized at that specific body site. A. baumannii were initially identified by API20E (Oxoid) and screened for resistance to either ceftazidime or ciprofloxacin using standard disc diffusion methods.14 All presumptive A. baumannii isolates were confirmed to the species level by the University of Michigan Clinical Microbiology Laboratory using matrix-assisted laser desorption ionization-time of flight mass spectrometry (Biotyper RUO; Bruker).37 Antimicrobial susceptibilities were verified by Vitek 2 using the GN82 AST (bioMérieux), according to Clinical
acinetobacter baumannii in nursing homes
and Laboratory Standards Institutes criteria and defined breakpoints.38 Tested antibiotic classes included (1) penicillin combinations (ampicillin/sulbactam and piperacillin/tazobactam); (2) aztreonam; (3) first-, third-, and fourthgeneration cephalosporins; (4) aminoglycosides (gentamicin and tobramycin); (5) quinolones (ciprofloxacin and levofloxacin); (6) carbapenems (imipenem and meropenem); (7) tetracycline; and (8) trimethoprim/sulfamethoxazole. Topical and antiseptic agents were not included in antimicrobial profiles. A. baumannii strains resistant to 3 or more classes of antibiotics were considered MDR.29 Statistical Analyses Data were entered into a master database (Access 2007; Microsoft) and analyzed using Stata, version 13.1 (StataCorp). The associations of key predictors with MDR A. baumannii colonization were examined using exact logistic regression adjusting for NH site to appropriately account for nesting and small sample sizes. Clustered logistic regression was used with exact logistic regression models for 2 reasons: (1) the clustered element was to account for the dependencies in the outcomes by facility, and (2) the exact logistic framework was used to address parameter estimation for small sample sizes. To explore more-complex associations among several predictors and MDR A. baumannii colonization, all prior statistically significant variables that had enough data were included in an augmented logistic model. The multivariable model was empirically driven on the basis of results from the previously run bivariate models using alpha ≤ .05.
results Study Population In the 6 control NHs, 215 residents or their legal guardian provided consent and were enrolled in the TIP study. No cases of MDR A. baumannii colonization occurred in 2 facilities, thus controls from these 2 NHs were excluded from further analysis (n = 47). The number of cases at the 4 remaining facilities varied, with facility E contributing the most (12 [48% of cases]) and facility G contributing the fewest (1 [4% of cases]). Facilities also differed in the degree of short- vs longterm care; the median length of stay among enrolled residents at facility K was 170 days compared with other facilities with median stays less than 90 days. Of the 168 residents with an indwelling device at 4 facilities, 25 (15%) were colonized at least once with MDR A. baumannii, all of which were resistant to cephalosporins, monobactam (aztreonam), and quinolones. Twenty-four cases (96%) carried A. baumannii resistant to 9 or more commonly used antibiotics. Most cases (20 [80%]) were colonized with carbapenem-resistant A. baumannii, accounting for 68.9% of isolates (93/135). Of the 25 cases, 16 (64%) were preexisting, or present on study enrollment, whereas 9 (36%) were new acquisitions. Eleven cases
1157
(44%) involved recurrent A. baumannii colonization and 14 (56%) were colonized on a single visit (Figure 1). Cases and controls were similar in baseline characteristics including age, sex, comorbidity score, rate of recent hospitalizations and antibiotic use, number of antibiotic classes used, and proportion of patients with urinary catheters (Table 1). Cases differed from controls in terms of functional disability, length of stay, total follow-up time, and presence of multiple indwelling devices. Cases had greater mean (SD) functional disability on average than controls (24.0 [3.8] vs 20.9 [4.5]), longer mean stays in the NH facility before enrollment (657 vs 133 days), and longer mean follow-up (151 vs 55 days). Risk Factors for MDR A. baumannii Colonization Clustered exact logistic regression models showed that colonization with MDR A. baumannii was significantly associated with functional disability. A high level of disability (PSMS score >24) was associated with a 4.3 times greater likelihood of MDR A. baumannii colonization (95% CI, 1.5–12.8; P < .006). Residents with both a feeding tube and urinary catheter were approximately 6 times more likely than residents with only one device to have MDR A. baumannii colonization (odds ratio, 6.1 [95% CI, 1.8–21.1]; P < .003). Diabetes was marginally associated with A. baumannii colonization (odds ratio, 2.9 [95% CI, 1.0–8.6]; P < .05). Co-colonization With Other AROs We evaluated the frequency of colonization with R-GNB, MRSA, and VRE prior to or concurrent with the first incidence of a positive MDR A. baumannii culture (Table 2). Of the 25 cases, 22 (88%) had at least one incidence of ARO colonization; Proteus mirabilis was the most prevalent organism among cases (56%), followed by VRE (48%), MRSA (44%), and Escherichia coli (44%). Of the 143 controls, 100 (70%) were colonized with at least one ARO during study follow-up; MRSA was the most prevalent organism among controls (43%), followed by VRE (25%), E. coli (23%), and P. mirabilis (17%). We were also interested in the frequency of co-colonization (ie, colonizing the same body site on the same visit) between MDR A. baumannii and other R-GNBs. Sixteen cases (64%) were considered to be co-colonized. Of 48 swab samples that indicated co-colonization, 30 (63%) revealed a single co-colonizing organism (in addition to A. baumannii) and 17 (35%) revealed 2 co-colonizing organisms. In one swab sample, MDR A. baumannii and antibiotic-resistant P. mirabilis, E. coli, and Morganella morgannii were all isolated from the perianal area of one resident. Table 3 describes the frequency of co-colonizing organisms isolated from 4 different body sites. Multivariable Model Examining A. baumannii Colonization We explored the association among several predictors that were significant in bivariate models and MDR A. baumannii
1158 infection control & hospital epidemiology
october 2015, vol. 36, no. 10
figure 1. Temporal trends of multidrug-resistant (MDR) Acinetobacter baumannii acquisition. Each row corresponds to a different nursing home resident and each column represents a follow-up visit. The mean length of stay prior to visit 0 among these residents was 657 days. White squares correspond to a follow-up day during which residents were not colonized with MDR A. baumannii; gray squares correspond to days in which swab specimens were not collected or days for which that resident was lost to follow-up. An X represents MDR A. baumannii colonization; an asterisk indicates recurrent MDR A. baumannii colonization.
table 1. Controls
Demographic Characteristics of Cases (With Multidrug-Resistant Acinetobacter baumannii Colonization) and
Characteristic Age, mean (SD), years Male sex History of MRSA History of VRE PSMS score, mean (SD) Comorbidity score, mean (SD) Device type at baseline Urinary catheter (UC) only Feeding tube (FT) only Both UC and FT Antibiotic usage within 30 daysa No. antibiotic classes used, mean (SD)b Hospitalization within 30 days Length of stay, mean, daysc Total follow-up, mean, daysd
Cases (n = 25)
Controls (n = 143)
P
68 (14) 16 (64) 7 (28) 1 (4) 24.0 (3.8) 3.7 (2.1)
70 (13) 83 (58) 25 (17) 14 (10) 20.9 (4.5) 3.0 (2.4)
.44 .58 .05 .68
