Chan, FHW

Chan, TC

Chen, JHK

Cheng, VCC

Chow, MK

Ho, PL

Law, TC

Ng, WC

So, SYC

Wong, JYH

Wong, SCY

Yuen, KY

Infection Control and Hospital Epidemiology

HKU Scholars Hub

TitleEmergence of Carbapenem-Resistant Acinetobacter baumanniiin Nursing Homes With High Background Rates of MRSAColonizationAuthor(s)Cheng, VCC; Chen, JHK; Ng, WC; Wong, JYH; Chow, MK; Law,TC; So, SYC; Wong, SCY; Chan, TC; Chan, FHW; Ho, PL; Yuen,KYCitation Infection Control & Hospital Epidemiology, 2016, v. 37 n. 8, p.983-986Issued Date 2016URL http://hdl.handle.net/10722/225635RightsInfection Control & Hospital Epidemiology. Copyright ©University of Chicago Press.; This work is licensed under aCreative Commons Attribution-NonCommercial-NoDerivatives4.0 International License.c on c i s e c ommun i c a t i o nEmergence of Carbapenem-ResistantAcinetobacter baumannii in Nursing HomesWith High Background Rates of MRSAColonizationVincent C. C. Cheng, MD;1,2 Jonathan H. K. Chen, PhD;1W. C. Ng,MBA(HSM);3 Janet Y. H.Wong, PhD;4 Denise M. K.Chow, PhD;4 T. C. Law, MSc(IC);3 Simon Y. C. So, MMedSc;1Sally C. Y. Wong, MD;1 T. C. Chan, MD;3 Felix H. W. Chan,MD;3 P. L. Ho, MD;1 K. Y. Yuen, MD1Carbapenem-resistant Acinetobacter baumannii (CRAB) with diversemultilocus sequence typing emerged among our nursing home resi-dents (6.5%) with a high background rate of MRSA (32.2%). Rectalswabs yielded a higher rate of CRAB detection than axillary or nasalswabs. Bed-bound status, use of adult diapers, and nasogastric tubewere risk factors for CRAB colonization.Infect Control Hosp Epidemiol 2016;37:983–986Transmission of multidrug-resistant organisms (MDROs) hasbeen increasingly reported in nursing homes.1,2 In HongKong, the prevalence of MRSA in nursing homes increasedfrom 2.8% to 21.6% between 2005 and 2011.3,4 Whileinfection control measures are generally more stringent inacute hospitals than in nursing homes, the latter have becomeepidemic centers for MDROs. With the emergence ofcarbapenem-resistant gram negative organisms in ourhospitals,5,6 it is important to determine the prevalence of andrisk factors for carbapenem-resistant Acinetobacter baumannii(CRAB), carbapenemase-producing Enterobacteriaceae(CPE), and other MDROs in our nursing homes includingmethicillin-resistant Staphylococcus aureus (MRSA) andvancomycin-resistant Enterococci (VRE). These ﬁndings areuseful in the formulation of infection control policy.methodsThis study was conducted from July 1, 2015, to August 31,2015, to determine the prevalence of MDROs among 28nursing homes in the Hong Kong West District with a popu-lation of 0.53 million. The role of nursing homes was describedpreviously.4 Trained research nurses collected nasal swabs,axillary swabs, and rectal swabs from consented subjects all onthe same day according to a standard protocol. The specimenswere tested by the microbiology laboratory for the presence ofCRAB, CPE, MRSA, and VRE as previously described.4–6 Thebacterial species were conﬁrmed by matrix-assisted laserdesorption/ionization time-of-ﬂight mass spectrometry(MALDI-TOF MS; Bruker Daltonics, Bremen, Germany).Susceptibility of the isolates was determined using theKirby–Bauer disc diffusion method or E test, and the resultswere interpreted according to the guidelines of the Clinical andLaboratory Standards Institute (CLSI). For molecular typing ofCRAB and MRSA, multilocus sequencing typing (MLST) andspa typing were performed on isolates of CRAB and MRSArespectively.6,7 Patient demographic data were retrieved andanalyzed. The χ2 test and Student t test were used as appropriatewith SPSS version 20 (IBM, Armonk, NY). Factors with P< .05in univariate analysis were chosen for multivariate analysis.A ﬁnal model was selected using a forward selection procedure.This study was approved by our institutional review board.resultsDuring the study period, 1,408 (60.6%) of 2,322 subjects from28 nursing homes consented to undergo screening. The meanage was 83.8± 10.3 years and 854 (60.7%) were female. Of 691(49.1%) residents who were functionally dependent, 474 of691 (68.6%) were chair bound and 217 of 691 (31.4%) werebed bound. Of 1,408 residents, 909 (64.6%) were incontinentrequiring the use of adult diapers; 62 (4.4%) had sacral sores;71 (5.0%) had nasogastric tubes; 4 (0.3%) had percutaneousgastrostomy tubes; 4 (0.3%) had Tenckhoff catheters; and75 (5.3%) had long-term urinary catheters.Overall, colonization of MDROs was found in 494 of 1,408residents (35.1%). MRSA colonization in any 1 of the 3 swabswas found in 454 residents (32.2%), while CRAB colonizationwas found in 92 residents (6.5%). A single resident had CPEwith NDM-1–producing E. coli. VRE was not detected in anyscreened specimens. Of the 1,408 residents, 399 (28.3%) werecolonized with MRSA only; 37 (2.6%) were colonized withCRAB only; and 55 (3.9%) were co-colonized with MRSA andCRAB. The subsequent analyses on residents focused on CRABand/or MRSA colonization because the number of residentswith CPE was small. The prevalence of CRAB and MRSAcolonization among residents through different body sites issummarized in Table 1.The univariate and multivariate analyses of the epidemio-logical risk factors for CRAB and MRSA colonization amongresidents in nursing homes are shown in Tables 2 and 3,respectively. Bed-bound status, incontinence with the use ofadult diapers, and presence of a nasogastric tube were thecommon risk factors for both CRAB and MRSA colonizationby multivariate analysis.Molecular characterization of CRAB and MRSA wasperformed in 25 and 30 non-duplicated patient isolates from6 nursing homes and showed a high prevalence of CRAB orMRSA respectively. A predominant spa type of MRSAt1081 was identiﬁed in 19 of 30 MRSA isolates (63.3%), ininfection control & hospital epidemiology august 2016, vol. 37, no. 8https://www.cambridge.org/core/terms. https://doi.org/10.1017/ice.2016.84Downloaded from https://www.cambridge.org/core. University of Hong Kong Libraries, on 08 Aug 2017 at 07:56:03, subject to the Cambridge Core terms of use, available atkeeping with the predominant MRSA clone of ST45/spa t1081in our locality.7 The MLST patterns of CRAB were diverse,including 8 of 25 clones of ST575 (32.0%), and 7 newlyreported MLST patterns in 7 patients with gastrointestinalcolonization of CRAB.discussionIn this study, we have demonstrated the emergence of CRABcolonization and a high prevalence of MRSA among nursinghomes residents in Hong Kong. The prevalence of CRABcolonization was 6.5%, almost 3 times higher than inhospitalized patients identiﬁed through active surveillanceculture in a previous study.8 The rate of CRAB was highestamong rectal swab cultures, which coincides with our previousﬁnding that residents in nursing homes have the most sig-niﬁcant risk factor for gastrointestinal colonization of CRABamong hospitalized patients.8 In our study, the burden ofantimicrobial-resistant A. baumannii was comparatively lesstable 2. Epidemiological Characteristics of Residents With or Without Colonization by Methicillin-Resistant Staphylococcus aureus(MRSA) and Carbapenem-Resistant Acinetobacter baumannii (CRAB)(A) Patients WithoutColonization by any MDROs,No. (%) (N= 914)a(B) Patients WithColonization byCRAB, No. (%)(N= 92)P Value (A)vs (B)(C) Patients WithColonization byMRSA, No. (%)(N= 454)P Value (A)vs (C)Age (mean years ± SD) 83.6± 10.2 81.8± 11.2 .107 84.5± 10.0 .111Male sex 358 (39.2) 56 (60.9) <.001 170 (37.4) .827Dependency: chair-bound 277 (30.3) 42 (45.7) .003 177 (39.0) .001Dependency: bed-bound 86 (9.4) 34 (37.0) <.001 119 (26.2) <.001Incontinence with adult diapers 509 (55.7) 84 (91.3) <.001 363 (80.0) <.001Presence of sacral sore 25 (2.7) 12 (13.0) <.001 31 (6.8) .001Presence of indwelling deviceNasogastric tube 18 (2.0) 14 (15.2) <.001 48 (10.6) <.001Percutaneous gastrostomy tube 1 (0.1) 1 (1.1) .127 3 (0.7) .161Urinary catheter 30 (3.3) 7 (7.6) .036 42 (9.3) <.001Underlying diseasesChronic cerebral conditions 119 (13.0) 33 (35.9) <.001 114 (25.1) <.001Chronic cardiac conditions 161 (17.6) 30 (32.6) <.001 139 (30.6) <.001Chronic pulmonary conditions 46 (5.0) 6 (6.5) .539 28 (6.2) .382Chronic renal failure 26 (2.8) 6 (6.5) .055 25 (5.5) .014Liver cirrhosis 13 (1.4) 1 (1.1) .794 4 (0.9) .395Diabetes mellitus 74 (8.1) 15 (16.3) .008 52 (11.5) .043Malignancies 27 (3.0) 7 (7.6) .019 22 (4.8) .076Use of antibiotic in preceding 6 monthsBeta-lactam/beta-lactamaseinhibitors33 (3.6) 15 (16.3) <.001 50 (11.0) <.001Cephalosporins 10 (1.1) 2 (2.2) .363 11 (2.4) .060Carbapenems 12 (1.3) 4 (4.3) .027 17 (3.7) .003Fluoroquinolones 29 (3.2) 10 (10.9) <.001 29 (6.4) .005History of hospitalization in thepast 6 months282 (30.9) 52 (56.5) <.001 220 (48.5) <.001aMDROs include methicillin-resistant Staphylococcus aureus, carbapenem-resistant Acinetobacter baumannii and carbapenemase-producingEnterobacteriaceae.table 1. Prevalence of Carbapenem-Resistant Acinetobacterbaumannii (CRAB) and Methicillin-Resistant Staphylococcus aureus(MRSA) Colonization Among Residents in Nursing Homes bySampling of Different Body SitesBody SitePrevalence ofCRABColonization, No.(%) (N= 1,408)Prevalence ofMRSAColonization, No.(%) (N= 1,408)Nasal swab 14 (1.0)a 265 (18.8)bAxillary swab 34 (2.4)a 129 (9.2)bRectal swab 64 (4.5)a 259 (18.4)bCombination of any 2 sitesNasal and/or axillary swabs 46 (3.3) 336 (23.9)Rectal and/or axillary swabs 83 (5.9) 315 (22.4)Rectal and/or nasal swabs 73 (5.2) 418 (29.7)Any one site 92 (6.5) 454 (32.2)aThe prevalence of CRAB colonization was statistically signiﬁcant bysampling of different body sites (P < .001).bThe prevalence of MRSA colonization was statistically signiﬁcant bysampling of different body sites (P < .001).984 infection control & hospital epidemiology august 2016, vol. 37, no. 8https://www.cambridge.org/core/terms. https://doi.org/10.1017/ice.2016.84Downloaded from https://www.cambridge.org/core. University of Hong Kong Libraries, on 08 Aug 2017 at 07:56:03, subject to the Cambridge Core terms of use, available atthan that in the United States, where 15% of high-risk nursinghome residents have been reported to be colonized withmultidrug-resistant A. baumannii (MRAB) using activesurveillance culture.2 Functional disability was an important riskfactor for MRAB colonization,2 and we further demonstratedthat physical dependency such as bed-bound status, incon-tinence requiring adult diapers, and nasogastric tube feedingwere signiﬁcant risk factors for CRAB colonization in ourmultivariate analysis. Unlike MRSA, for which a predominantspa type prevailed, CRAB isolated from nursing home residentshad diverse MLST patterns. This ﬁnding contrasts with theobservation of clonal dissemination of A. baumannii inhospitals,6 suggesting that a successful clone of A. baumannii hasnot yet been established in these nursing homes.In this study, the prevalence of MRSA colonization amongelderly residents in nursing homes was 32%, which was10 times higher than the prevalence reported in Hong Kong10 years ago.3 The predominant spa type of MRSA was t1081,which was also the most commonly identiﬁed spa type amongthe hospital isolates.7 Notably, the rate of gastrointestinalcolonization of MRSA was as high as nasal colonization amongour residents. Widespread environmental contamination hadbeen shown previously in patients with MRSA colonization ofthe gastrointestinal tract.9 This factor may explain why MRSAin nursing homes could not be brought under control.With the emergence of CRAB and increasing prevalence ofMRSA colonization in our nursing homes, it is important toenhance infection control interventions. Active surveillanceculture may facilitate early recognition of residents colonizedwith MDROs. In our analysis, collection of nasal swabs andrectal swabs, even without axillary swabs, detected 80% and92% of CRAB and MRSA, respectively. Hand hygiene byhealthcare workers (HCWs) in nursing homes should beenforced. In particular, supervisors of nursing homes shoulddirectly observe and ensure the implementation of handhygiene practices by HCWs during and after adult diaperchanges and feeding via nasogastric tubes because these weresigniﬁcant risk factors for CRAB and MRSA colonization inour study. Additionally, directly observed hand hygiene beforemeals and oral medication administration by conscious resi-dents should be promoted to prevent ingestion of MDROs intothe gastrointestinal tract.6,10We are aware of several limitations in this study. First, wedid not screen patients who were demented or mentallyincapacitated and had not undergone interval screening. Bothof these factors may have led to the underestimation ofMDRO prevalence. Second, we did not assess the degree ofenvironmental contamination, and gastrointestinal colonizationof MRSA was associated with signiﬁcant environmental con-tamination.9 Third, we selected CRAB and MRSA strains fromnursing homes with high incidence, which may have led to theoverrepresentation of “epidemic clones.” However, our ﬁndingshighlight the rapid emergence of CRAB in nursing homes, whichdeserves the attention of infection control professionals.acknowledgmentsFinancial support: This study was partially supported by the Health andMedical Research Fund (HMRF), Food and Health Bureau, Hong Kong SARGovernment (grant no. HKM-15-M12).Potential conﬂicts of interest: All authors report no conﬂicts of interestrelevant to this article.Afﬁliations: 1. Department of Microbiology, Queen Mary Hospital, HongKong Special Administrative Region, China; 2. Infection Control Team,Queen Mary Hospital, Hong Kong Special Administrative Region, China;3. Community Geriatric Assessment Team, Fung Yiu King Hospital, HongKong Special Administrative Region, China; 4. School of Nursing, TheUniversity of Hong Kong, Hong Kong Special Administrative Region, China.Address correspondence to KY Yuen, Department of Microbiology, QueenMary Hospital, Hong Kong Special Administrative Region, China(kyyuen@hku.hk).Received December 10, 2015; accepted March 11, 2016; electronicallypublished April 25, 2016© 2016 by The Society for Healthcare Epidemiology of America. All rightsreserved. 0899-823X/2016/3708-0017. DOI: 10.1017/ice.2016.84references1. D’Agata EM, Habtemariam D, Mitchell S. Multidrug-resistantGram-negative bacteria: inter- and intradissemination amongtable 3. Risk Factors in Residents With Colonization by Carbapenem-Resistant Acinetobacter baumannii (CRAB) and Methicillin-Resistant Staphylococcus aureus (MRSA) Using Multiple Logistic RegressionaColonization by CRAB Colonization by MRSACharacteristic Odds Ratio (95% CI) P Value Odds Ratio (95% CI) P ValueDependency: bed-bound 2.70 (1.52–4.79) .001 2.50 (1.66–3.77) <.001Incontinence with adult diapers 5.01 (2.30–10.92) <.001 1.78 (1.26–2.52) .001Presence of nasogastric tube 2.98 (1.25–7.09) .014 2.64 (1.45–4.77) .001Presence of chronic cerebral conditions NS NS 1.55 (1.13–2.11) .006Use of beta-lactam/beta-lactamase inhibitors in preceding 6 months NS NS 2.34 (1.44–3.82) .001NOTE. CI, conﬁdent interval.aAll epidemiological characteristics listed were used as independent variables. Final model was selected using a forward selection procedure. Forthe analysis of CRAB colonization, the Hosmer-Lemeshow goodness-of-ﬁt statistic was 4.17, and P= .841. For the analysis ofMRSA colonization,the Hosmer-Lemeshow goodness-of-ﬁt statistic was 3.23, and P= .780.carbapenem-resistant a. baumannii in nursing homes 985https://www.cambridge.org/core/terms. https://doi.org/10.1017/ice.2016.84Downloaded from https://www.cambridge.org/core. University of Hong Kong Libraries, on 08 Aug 2017 at 07:56:03, subject to the Cambridge Core terms of use, available atnursing homes of residents with advanced dementia. InfectControl Hosp Epidemiol 2015;36:930–935.2. Mody L, Gibson KE, Horcher A, et al. Prevalence of and riskfactors for multidrug-resistant Acinetobacter baumanniicolonization among high-risk nursing home residents. InfectControl Hosp Epidemiol 2015;36:1155–1162.3. Ho PL, Wang TK, Ching P, et al. Epidemiology and geneticdiversity of methicillin-resistant Staphylococcus aureus strains inresidential care homes for elderly persons in Hong Kong. InfectControl Hosp Epidemiol 2007;28:671–678.4. Cheng VC, Tai JW, Wong ZS, et al. Transmission of methicillin-resistant Staphylococcus aureus in the long-term care facilities inHong Kong. BMC Infect Dis 2013;13:205.5. Ho PL, Cheung YY, Wang Y, et al. Characterization ofcarbapenem-resistant Escherichia coli and Klebsiella pneumoniaefrom a healthcare region in Hong Kong. Eur J Clin MicrobiolInfect Dis Jan 6 2016, [Epub ahead of print].6. Cheng VC, Chen JH, Poon RW, et al. Control of hospitalendemicity of multiple-drug-resistant Acinetobacter baumanniiST457 with directly observed hand hygiene. Eur J Clin MicrobiolInfect Dis 2015;34:713–718.7. Gruteke P, Ho PL, HaenenA, LoWU, LinCH, deNeeling AJ.MRSAspa t1081, a highly transmissible strain endemic to Hong Kong,China, in the Netherlands. Emerg Infect Dis 2015;21:1074–1076.8. Cheng VC, Chen JH, So SY, et al. Use of ﬂuoroquinolones is thesingle most important risk factor for the high bacterial load inpatients with nasal and gastrointestinal colonization bymultidrug-resistant Acinetobacter baumannii. Eur J Clin MicrobiolInfect Dis 2015;34:2359–2366.9. Boyce JM, Havill NL, Otter JA, Adams NM. Widespread envir-onmental contamination associated with patients with diarrheaand methicillin-resistant Staphylococcus aureus colonization ofthe gastrointestinal tract. Infect Control Hosp Epidemiol2007;28:1142–1147.10. Cheng VC, Tai JW, Wong LM, et al. Effect of proactive infectioncontrol measures on benchmarked rate of hospital outbreaks: Ananalysis of public hospitals in Hong Kong over 5 years. Am J InfectControl Jun 6 2015, [Epub ahead of print].986 infection control & hospital epidemiology august 2016, vol. 37, no. 8https://www.cambridge.org/core/terms. https://doi.org/10.1017/ice.2016.84Downloaded from https://www.cambridge.org/core. University of Hong Kong Libraries, on 08 Aug 2017 at 07:56:03, subject to the Cambridge Core terms of use, available at

Emergence of Carbapenem-Resistant Acinetobacter baumannii in Nursing Homes With High Background Rates of MRSA Colonization

Emergence of Carbapenem-Resistant Acinetobacter baumannii in Nursing Homes With High Background Rates of MRSA Colonization

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