GUIDELINES ARTICLE Open Access

Recommendations for the surveillance ofmultidrug-resistant bacteria in Italian long-term care facilities by the GLISTer workinggroup of the Italian Association of ClinicalMicrobiologists (AMCLI)Richard Aschbacher1, Leonardo Pagani2* , Roberta Migliavacca3, Laura Pagani3 and the GLISTer (Gruppo diLavoro per lo Studio delle Infezioni nelle Residenze Sanitarie Assistite e Strutture Assimilabili) working group

Abstract

Long-term care facilities (LTCFs) are an important reservoir of multidrug-resistant organisms (MDROs). Colonizationof LTCF residents by MDROs is generally higher in Italy compared to other European countries. The present reviewby the working group for the study of infections in LTCFs (GLISTer) of the Italian Association of Clinical Microbiologists(AMCLI) aims to propose criteria for a laboratory-based surveillance of MDROs in Italian LTCFs.We recommend the adhesion to three levels of laboratory-based MDROs surveillance in LTCFs: i) mandatory MDROsurveillance by cumulative retrospective analysis of antimicrobial susceptibility data, obtained as part of routine care ofclinical specimens. ii) strongly recommended surveillance by active rectal swab cultures or molecular screening todetermine colonization with carbapenemase-producing Enterobacterales, should a resident be proven infected. iii)voluntary surveillance by prospective MDRO surveys, mainly based on point prevalence colonization studies, allowingto determine the MDROs baseline prevalence in the facility.Laboratory-based surveillance of MDROs in LTCFs is aimed at providing useful epidemiological information tohealthcare providers operating in the facility, but it is only effective if the collected data are used for infectionprevention and control purposes, targeting the peculiar aspects of LTCFs.

Keywords: Italy, LTCF, MDRO, Surveillance, Screening, Infection control, Prevention

IntroductionLong-term care facilities (LTCFs) are institutions thatprovide skilled nursing care to residents in need of as-sistance with activities of daily living. LTCFs encompassnursing homes, residential care centers, chronic diseasehospitals, rehabilitation centers and institutions formentally handicapped persons [1]. These facilities are

functionally the home for residents, usually elderly andin declining health status, often staying for months toyears. Due to the ageing population in Italy (present lifeexpectancy 80.1 years for males and 84.7 years forfemales) LTCFs play an important role in the Italianhealthcare system; in December 2013, 12.200 LTCFswere counted, hosting 384.000 people, and these figuresare intended to increase during the next decades[http://www.istat.it/].The frequently older, sicker residents cared for in

LTCFs, have a variety of risk factors for colonization and

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* Correspondence: lpagani.id@gmail.com2Infectious Diseases Unit, Bolzano Central Hospital, Bolzano, ItalyFull list of author information is available at the end of the article

Aschbacher et al. Antimicrobial Resistance and Infection Control (2020) 9:106 https://doi.org/10.1186/s13756-020-00771-0

infection by multidrug-resistant organisms (MDROs).Pathogen cross-transmission within LTCFs is a signifi-cant issue and residents of these facilities are frequentlymoved between the acute and the long-term care set-tings [2]. For these reasons, LTCFs are an important res-ervoir for MDROs, such as methicillin-resistantStaphylococcus aureus (MRSA), vancomycin-resistantenterococci (VRE), Pseudomonas aeruginosa or Acineto-bacter baumannii with MDR phenotypes (expressing re-sistance to ≥3 classes of antibiotics) and Enterobacteralesproducing extended-spectrum β-lactamases (ESBLs),high-level cephalosporinases (AmpCs) and/or carbape-nemases [3, 4]; these MDROs have been included in thepresent surveillance recommendations.Surveillance of MDROs in a healthcare institution is of

pivotal importance for guiding prevention, therapy andcontrol of infectious diseases caused by these organisms[5]. The urgent need for MDRO surveillance recommen-dations in Italian LTCFs has been highlighted during theNational Congress of AMCLI in Rimini, 2017 [6], and bythe national plan for contrasting antimicrobial resistance2017–20, approved by the Italian Presidency of theCouncil of Ministers (PNCAR) [7]. Therefore, the Italianworking group for the study of infections in LTCFs(GLISTer) of the Association of Italian Clinical Microbi-ologists (AMCLI), has been prompted to define and rec-ommend general indications for the surveillance ofMDROs in Italian LTCFs [8]. For literature search weadopted a search strategy in the Medline/Pubmed data-base including the following search terms: (nursinghome* OR long term care facility*) AND (colonizationOR multi drug resistan* OR ESBL OR MRSA OR VREOR carbapenemase*) AND Italy. We restricted thesearch to the dates range 01.01.2000–30.08.2019 but didnot impose any language restriction. Applying thissearch strategy, we identified 30 articles; from the refer-ence lists of the above articles we retrieved further stud-ies. Moreover, we included a Poster Abstract from theNational Congress AMCLI 2017, the “Piano Nazionaleper il Contrasto dell’antimicrobico-resistenza 2017-20(PNCAR)”, Clinical and Laboratory Standards Institute(CLSI) guidelines for analysis and presentation of cumu-lative antimicrobial susceptibility test data, and inter-national and national guidelines for infection preventionand control in LTCFs. At least two authors screenedevery abstract and full-text article or guideline, the re-sults have been collegially discussed before the inclusionin the review article.The recommendations are intended to be used by local

and regional bodies, comprising LTCF physicians, infec-tious disease specialists and nurses, infection prevention-ists, LTCF administrations, referral hospital physicians,clinical microbiologists and administrations.

MDR bacteria in Italian LTCFsDwelling in a LTCF is an independent risk factor forbloodstream infections by MDROs [9], and Italy has oneof the highest prevalence of MDROs isolated from bloodcultures in European countries, especially for MRSA,carbapenemase-producing A. baumannii and ESBL- orcarbapenemase-producing Enterobacterales (CPE) [10].A systematic review of studies on colonization byMDROs from Italian LTCFs, on risk factors forcolonization and on molecular characteristics of clinicalisolates also in comparison with other European coun-tries, has been published recently [11]. Italian reviewdata show an MRSA colonization prevalence of 7.8–38%for residents and 5.2–7.0% for staff members, an ESBL-prevalence of 50–64% for residents and 5.2–14% for staffand a CPE-prevalence of 1.0–6.3% for residents and 0.0–1.5% for staff. These data show that colonization of resi-dents in Italian LTCFs is generally significantly higherthan in other European countries. A point prevalencesurvey undertaken in 2008 in an Italian LTCF [12], re-peated in 2012 [13] and 2016 [14], showed high residentcolonization rates for ESBL-producing Enterobacterales(49.0–64.0%), a low prevalence for CPE (1.7–6.3%) and avariable prevalence for MRSA-colonization (13.2–38.7%).Two recent multicenter studies in Italian LTCFs, con-firmed a high colonization prevalence (ranging from 32.8to 81.5%) for ESBL-producing Enterobacterales, especiallyEscherichia coli, whereas lower prevalence was found forCPE (0.0–5.8%) and carbapenemase-producing A. bau-mannii (0.0–5.8%); highly variable prevalence was foundfor MRSA (5.0–30.6%) and VRE (0.8–20.2%) [15, 16].An Italian multicenter study, investigating the fre-

quency of ESBL-producing Enterobacterales in urinespecimens from LTCF residents, found a median ESBL-rate of 32.1%, with E. coli as the most frequent ESBL-producing pathogen [17].In Italian LTCFs, as well as in other European coun-

tries, the most prevalent ESBLs from E. coli isolates werefound CTX-M-type enzymes, particularly CTX-M-15,mainly belonging to the pandemic ST131 clonal group[11, 15, 18]. On the other hand, carbapenemases inEnterobacterales from Italian LTCFs, generally are ofKPC- or VIM-type [11, 15, 16]. Recently, other authors re-ported a high colonization rate of residents with KPC-type-producing Klebsiella pneumoniae in a LTCF from centralItaly: 11.6% of patients were colonized at admission, 9.9%subsequently, with very high rates of carriage and cross-transmission in severe brain injury patients [19].It is important to emphasize that published surveil-

lance studies from Italian LTCFs are scarce. Moreover,large urban facilities are overrepresented, and there havebeen no systematic, culture-based or molecular surveysat national or regional level until now.

Aschbacher et al. Antimicrobial Resistance and Infection Control (2020) 9:106 Page 2 of 12

Surveillance recommendations for MDROs inItalian LTCFsRecommended laboratory based surveillance strategiesfor MDROs range from passive surveillance of routineclinical microbiology laboratory-results (1st level) [20],up to retrospective (2nd level) [2] or prospective surveil-lance screening (3rd level) [21].

Surveillancelevel

Strategies Organismsincluded

Recommendation Limitations

1st levellaboratorybasedsurveillance

Surveillanceof routineclinicalmicrobiologylaboratory-results

VariousMDROs

Mandatory Low numberof collectedsamples,identificationof specimensas comingfrom LTCFpatients,exclusion ofcolonizationdata

2nd levellaboratorybasedsurveillance

Activesurveillancecultures

GenerallyCPE,possibleextensionto otherMDROs

Stronglyrecommended

Generallylimitation tocolonizationby CPE,exclusion ofroutineisolates frominfections

3rd levellaboratorybasedsurveillance

Prospectivefacilityscreeningof LTCFresidentsfor MDROs

VariousMDROs

On a voluntarybasis, andrecommended

Generallypointprevalencestudy, exclusionof routineisolates frominfections,costlyand time-consuming

Variation in MDRO surveillance includes facility widevs. targeted units, patient based vs. laboratory based,colonization vs. infection, passive vs. active, retrospectivevs. prospective, and optional vs. required strategies. Thesignificant heterogeneity of Italian LTCFs, as referred tobed number, resident comorbidities and staffing, and theheterogeneity of local, regional and national regulations,complicate the recommendation of generally acceptablesurveillance measures for MDROs [7]. Laboratory-basedsurveillance of MDROs should be associated to a carefulinfection monitoring -e.g. of incidence of urinary tractinfections or central line associated bacteremia-, byhealthcare providers within the LTCF, and should alsobe paralleled by evaluation of the consumption of antibi-otics in the institution, as key prerequisites for the im-plementation of an infection control and antimicrobialstewardship programs [22, 23]. In any case, routine en-vironmental cultures or samples from asymptomatic

personnel are not recommended, except as target for anepidemiologic investigation.

Surveillance of routine clinical microbiologylaboratory-results (first level laboratory-basedsurveillance, mandatory)We define first level surveillance of MDROs in LTCFs asthe cumulative retrospective analysis of antimicrobialsusceptibility data, obtained as part of routine care fromdiagnostic cultures of clinical specimens in the referringclinical microbiology laboratory, in accordance with theClinical Laboratory Standards Institute (CLSI) guidelinefor recording and analysis of antimicrobial susceptibilitydata [5]. Local susceptibility data are mainly used toprovide useful information to enable laboratories toassist the clinician in the selection of appropriatetherapy for infections, but they can also be used as abasis for infection prevention and control procedures.Microbiology laboratories chosen by LTCFs for

analysis of microbiological specimens must comply withthe following criteria:

� accreditation/certification for the analysis ofmicrobiology samples, including implementation ofthe required internal and external quality controlprograms

� documentation of an adequate volume of sampleprocessing activity

� capability of cryopreservation of MDR organisms� ability to collect, elaborate and present cumulative

antibiotic susceptibility data

Therefore, specimen processing and data elaborationin a few regional reference laboratories is recommended:it facilitates standardized cumulative retrospectiveanalysis of antimicrobial susceptibility data and theircomparison among different LTCFs.A major disadvantage of using such retrospective

susceptibility data is the generally low number ofspecimens sent to the clinical microbiology laboratory,limiting the number of isolates available forsusceptibility testing and cumulative analysis. Therefore,combining of data from consecutive years (e.g. 3 years)and from several comparable LTCFs in a healthcaredistrict area may be required [5]. Elaboration of suchcombined data is useful for indication of general trends,which can be compared with outpatient or acute-carehospital (ACH) inpatient data from the same geographicregion [5]; however, if data are pooled from consecutiveyears, changes in resistance profiles might be difficult todetect. For example, selective cumulative susceptibilitydata on routine clinical isolates from LTCFs, inpatientsand outpatients from the Bolzano healthcare district,highlighted significantly higher rates of MRSA and

Aschbacher et al. Antimicrobial Resistance and Infection Control (2020) 9:106 Page 3 of 12

cefotaxime-resistance in E. coli (mainly ESBL-producers)from LTCF residents, compared with isolates from hos-pital inpatients; this was not the case for cefotaxime- ormeropenem-resistance in K. pneumoniae or formeropenem-resistance in P. aeruginosa (Fig. 1).Therefore, an essential requirement for an efficient

laboratory-based passive MDROs surveillance system is themandatory collection of specimens for diagnostic microbio-logical testing during infectious episodes. Moreover, becauseof the generally low number of isolates, we recommend toalways calculate the 95% confidence interval for antimicro-bial resistance rates. Together with the cumulative retro-spective analysis of antimicrobial resistance data, a line

listing of residents infected/colonized with MDROs shouldbe provided to the infection control practitioners operatingin the LTCFs; the line listing can also be prepared for lowisolate numbers of single MDRO species (< 30 isolates).Various criteria for exclusion of multiple isolates of

the same species from single patients have beenproposed [5]. The frequently used first isolate perepisode based calculation, includes the first isolate of agiven species recovered from each episode of infection,and an episode is defined as the set of all isolates from apatient in which the interval between consecutiveisolates is less or equal to a defined time interval, e.g. 28days. In order to analyze the effect of removal of duplicate

Fig. 1 Antibiotic resistance in routine clinical isolates from LTCFs, hospital inpatients and outpatients in the Bolzano healthcare district. Resistancerates were calculated using episode based duplicate exclusion within 28 days (Virtuoso Plus, Dedalus Healthcare Systems Group, Florence, Italy).Screening isolates have been excluded. MRSA: methicillin-resistant S. aureus, CTX: cefotaxime, MEM: meropenem. Error bars: 95% confidenceinterval (https://www.graphpad.com/). Number of isolates: S. aureus (LTCFs: 56; inpatients: 1187; outpatients: 918), E. coli (LTCFs: 430; inpatients:3202; outpatients: 6202), K. pneumoniae (LTCFs: 84; inpatients: 844; outpatients: 874), P. aeruginosa (LTCFs: 96; inpatients: 723; outpatients: 477)

Fig. 2 Antibiotic resistance dependent on the method of duplicate isolate removal. Resistance rates were calculated using different methods ofduplicate isolate removal (Virtuoso Plus, Dedalus Healthcare Systems Group, Florence, Italy). Screening isolates have been excluded. MRSA:methicillin-resistant S. aureus, CTX: cefotaxime, MEM: meropenem. Error bars: 95% confidence interval (https://www.graphpad.com/). Number ofisolates (from left to right): S. aureus (62–57–57-57-56-54-52), E. coli (451–444–444-443-430-393-345), P. aeruginosa (105–103–102-99-96-90-80)

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isolates by an episode based strategy, we considered alldiagnostic isolates (active surveillance isolates excluded)recovered during 2015–17 from LTCF residents in theBolzano healthcare district, and generated cumulativesusceptibility reports for MRSA, cefotaxime-resistant E.coli and meropenem-resistant P. aeruginosa, based on theall isolates strategy and on different episode-based strat-egies (minimal interval of time: 2, 7, 14, 28, 100 or 360days) (Fig. 2). Of note, though a considerable percentageof isolates was removed from calculation in the episodebased strategy, with a minimal time interval of 360 days,compared to the all isolates approach (MRSA: 16.1%, E.coli: 23.5%, P. aeruginosa: 16.4%), the multiple isolates re-moval did not significantly change resistance rates. Similarstudies on the effect of duplicate isolates removal may leadto varying results, depending not only on the method usedfor the exclusion of multiple isolates, but also on local epi-demiology, sampling practice and patient demographics[24]. Recommendations for the application of various epi-sode based duplicate exclusion strategies have been pub-lished; it was found that cumulative antimicrobialsusceptibility reports based on a 28 days’ episode strategy,reflect resistance rates among hospital-acquired infections[25]. A similar duplicate exclusion strategy has thereforebeen proposed by an Italian guideline [26]; other authorsconsider a 10 days episode strategy as first choice for thehospital inpatient setting [24]. LTCF residents stay in thefacility for months or years and, due to their underlyingchronic diseases, MDROs can give repeatedly rise to infec-tions, requiring frequent antimicrobial treatments. Forthese reasons, we recommend a 28 days’ episode basedstrategy for multiple isolates from LTCF residents, but itshould be emphasized that the time interval chosen doesnot significantly change the obtained susceptibility rates;moreover, a 28 days’ episode based exclusion strategy forduplicate isolates has recently been adopted for blood cul-ture isolates by the Italian PNCAR [8].It is essential that clinical specimens from LTCF

residents are clearly associated to a specific LTCF, butthis is not always the case in Italian LTCFs; mixingLTCF data with those of ambulatory patients is a majormistake when it comes to tracing the epidemiology ofantimicrobial resistance [20].Patients hospitalized in an LTCF are sometimes

transferred to the referral ACH for treatment of seriousinfections and then they undergo diagnostic cultures ofclinical specimens; it is generally a difficult datamanagement problem to include these isolates in the 1stlevel LTCF surveillance, but results of these cultures shouldnot be missed, as they represent the most serious infectiousepisodes. A proposed solution to this limitation is tointegrate the 1st level LTCF surveillance into the generalcumulative antimicrobial susceptibility report, stratifyingdata according to outpatients, patients hospitalized in the

referral ACH and LTCF residents; isolates from residents inLTCFs and from residents admitted to the referral ACH(within 48 h) should, if possible, be pooled together in thedrafting of the report.Based on published international and national

guidelines [5, 20, 27], and applying various modificationsfor LTCFs, for the mandatory first level laboratory-basedMDROs surveillance in LTCFs we suggest the followingrecommendations and strategies.

Theme of therecommendation

Recommendedstrategies

Comments Specificresponsibilities

Microbiologicalspecimencollection

Require fromLTCF healthcareproviders themandatorycollection ofspecimens formicrobiologicaltesting duringinfectiousepisodes inLTCF residents

Essential forempirictherapyand forinfectioncontrol

LTCF physicians,nurses, LTCFinfectionpreventionists

Microbiologylaboratoryselection

Selectlaboratoriesaccredited/certified foranalysis ofmicrobiologicalspecimens thatare alsoequippedfor long-termcryopreservationof MDRO isolatesand for thecollection,elaboration andpresentation ofantibioticsusceptibilitydata

Preferablychoose afew regionalreferencelaboratories

LTCFadministration,clinicalmicrobiologists

Communication Communicateimmediatelythe isolation ofMDROs fromLTCF residents toinfection controlpractitioners inthe LTCFs (byphone, fax,e-mail, orsmartphonemessage) andby preliminaryreporting

Applicationof the internalprotocol forcommunicationof laboratory-results (e.g.MRSA, VRE, P.aeruginosa orA. baumanniiwith MDRphenotypeandEnterobacteralesproducing ESBLs,high-levelAmpCs and/orcarbapenemases)

Clinicalmicrobiologists,LTCF physicians,LTCF infectionpreventionists

Data elaboration Producecumulativeantibiogramsannually andseparately foreach LTCF if asufficient

If the numberof isolates perspecies and yearis < 30, extendthe time periodup to 3 yearsand/or include

Clinicalmicrobiologistsand/orepidemiologists

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Surveillance of routine clinical microbiology laboratory-results (first level laboratory-based surveillance,mandatory) (Continued)

number ofisolates perspecies andyear is available(≥30 isolatesper species)

severalcomparableLTCFs inthe samegeographicarea, inagreementwith theinfectioncontrolpractitionersin the involvedLTCFs.Prepare forisolate numbers< 30 for singlebacterial speciesa line listing ofidentified MDROs

Data elaboration Exclude isolatesfrom activesurveillanceand screeningstudies fromthe cumulativeantibiogramsand, if available,elaborate thisdata separately

Elaboratesurveillanceand screeningdata separately(see surveillancelevels 2 and 3)

Clinicalmicrobiologistsand/orepidemiologists

Data elaboration Calculateantimicrobialsusceptibilityrates at specieslevel, focusingon the mostimportantresistancephenotypes

Include at leastS. aureus (MRSA),E. faecalis and E.faecium (VRE),E. coli andK. pneumoniae(ESBL,carbapenemases),P. aeruginosaandA. baumannii(carbapenem-resistance,carbapenemases)

Clinicalmicrobiologistsand/orepidemiologists

Data elaboration Adhere to theEuropeanCommittee onAntimicrobialSusceptibilityTesting(EUCAST)recommendationsto ensurestandardizedantimicrobialsusceptibilitytesting

Disclose anychangein antimicrobialsusceptibilitytestingmethodologyandinterpretativereading(for exampletherapeuticcorrectionof cephalosporininterpretation forESBL producers)

Clinicalmicrobiologistsand/orepidemiologists

Data elaboration Use an episode-based strategyfor exclusion ofmultiple isolatesper resident,with a minimumdefault interval

Discuss differentother possibleremovalstrategiesfor duplicateisolateswith the LTCF

Clinicalmicrobiologistsand/orepidemiologists,LTCF infectioncontrolpractitioners

Surveillance of routine clinical microbiology laboratory-results (first level laboratory-based surveillance,mandatory) (Continued)

of timebetween theirrecovery of28 days

infection controlpractitioners.Define anddisclosethe calculationalgorithm usedfor cumulativeantimicrobialsusceptibilitytest reports

Data elaboration Use stratificationof data byspecimen type(for exampleurine, blood,others) only ifsufficiently highisolate numbers(≥30 isolatesper species andspecimensubgroup)have beentested

Discuss variousdatastratificationoptions withthe infectioncontrolpractitionersin the LTCF

Clinicalmicrobiologistsand/orepidemiologists,LTCF infectioncontrolpractitioners

Data elaboration Calculate thepercentage ofMDRO-isolates/total number ofisolates × 100(applying a28 days’ episodebased multipleisolates exclusionstrategy)

Always add95% confidenceintervals tosusceptibilityrates

Clinicalmicrobiologistsand/orepidemiologists

Data elaboration Integrate theLTCF surveillancereport into ageneralcumulativeantimicrobialsusceptibilitydata report,comparingisolates fromLTCF residentswith outpatientisolates andisolates fromreferral acutecare hospitalpatients

If possible,stratifyisolates fromLTCF residentsadmittedwithin 48 hto the referralACH togetherwith LTCFisolates

Clinicalmicrobiologistsand/orepidemiologists

Data reporting Reportantimicrobialsusceptibilityrates only forantibioticsroutinely testedon all isolates

Do not reportsupplementalantimicrobialagents thatare selectivelytested onresistantisolates

Clinicalmicrobiologistsand/orepidemiologists

Data reporting Reportantimicrobialsusceptibilitydata aspercentages

According toEUCASTcriteria

Clinicalmicrobiologistsand/orepidemiologists

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Surveillance of routine clinical microbiology laboratory-results (first level laboratory-based surveillance,mandatory) (Continued)

of susceptible-standard dosingregimen,susceptible-increasedexposureand resistantisolates

Data reporting Present thereport preferablyin a graphicformat, easilyaccessible tothe healthcarepractitioners inthe LTCFs, forexample on theinstitution’swebsite

Discuss datawithhealthcareproviders inthe LTCFs

Clinicalmicrobiologistsand/orepidemiologists,healthcareproviders inLTCFs

Isolateconservation

CryopreserveMDR-isolates(at −80 °C)

Preserve forfurthermolecularcharacterization,in collaborationwith a referencemolecularbiologylaboratory

Clinicalmicrobiologists

Surveillance by active surveillance cultures(second level laboratory-based surveillance,strongly recommended)Active surveillance of LTCF residents for carriage ofMDROs can be defined as obtaining isolates fromcultures of specimens that are collected for determiningif a patient is harboring a particular organism, and arenot from cultures that are obtained as part of the clinicalevaluation of a resident’s illness. Active surveillancecultures are specifically designed for MDROs, for whichusual reservoirs are established and validated screeningtests are available, e.g. CPE [28]. Active surveillance ofMDROs can also be based on molecular amplificationmethods. Use of active surveillance has been shown toimprove detection of MDROs, compared with relianceon culture of specimens collected for clinical reasonsalone [29].Specimen types used for active MDRO-screening may

influence surveillance data. ESBL- and carbapenemase-producing Enterobacterales and VRE are most often re-covered from rectal samples (possibly combined withurine samples), whereas we have shown that for MRSA-screening a combination of oropharyngeal (or nasal) andinguinal (or perineal) swabs gives highest yields; testingof only nasal swabs results in substantial underestima-tion of colonization with MRSA [12–14]. Forcarbapenem-resistant P. aeruginosa and A. baumannii

oropharyngeal and rectal swabs are recommended (pos-sibly combined with urine samples) [16, 30–32].According to LTCF infection prevention and control

guidelines active surveillance of MDROs in LTCFs byculture methods or by using molecular amplificationassays should not imply routine screening of residents atthe time of admission to the facility, nor should it berepeated on a periodic basis, in the absence of anepidemic of infections by MDROs, because the applicationof standard precautions, as applied to all residents, issufficient [2]. Active surveillance screening for variousMDROs should be individualized to residents at risk forshedding large numbers of bacteria into the environment,e.g. residents with colonized wounds not covered fullywith dressings, incontinent residents with urinary or fecalcarriage, or residents with tracheostomies and difficulty inhandling respiratory secretions [1].CPE, especially KPC-producing K. pneumoniae, are ep-

idemically spread in Italy [10, 33] and the emergence ofthis MDR-phenotype in LTCFs is widely expanding thereservoir of this health-care threat [11, 15, 16, 19]. Basedon the current epidemiology and the clinical significanceof CPE, we recommend targeting active MDROs surveil-lance screening in Italian LTCFs on CPE, according toAMCLI indications for the screening of carbapenemasesin Enterobacteriales [28]; identification of the main car-bapenemase types in Italy (KPC, OXA-48-like, VIM,NDM) by antigenic or molecular methods is essential.Though active surveillance in Italian LTCFs is generallyrestricted to CPE, in accordance with healthcare pro-viders in the LTCFs and taking into consideration thevarious levels of complexity of the single LTCF, otherMDROs may be considered for screening.GLISTer recommends active routine surveillance

screening of MDROs in LTCFs as follows.

Theme of therecommendation

Recommendedstrategies

Comments Specificresponsibilities

Selection ofMDRO types

Generally restrictactive MDROsurveillancescreening toCPE

In accordancewith healthcareproviders in theLTCFs, otherMDROs may beconsidered forscreening

LTCF physicians,LTCF infectionpreventionists,clinicalmicrobiologists

Selection ofLTCF residents

Perform activesurveillancecultures (ormolecularscreening) inthe presenceof infectionby CPE (indexcase), excludingcolonizationsuch asasymptomaticbacteriuria

Screening isespeciallyrecommended ifthe index case isat risk forshedding largenumbers ofbacteria into theenvironment,e.g. residentswith colonizedwounds not fullycovered with

LTCF physicians,LTCF infectionpreventionists,Clinicalmicrobiologists

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Surveillance by active surveillance cultures (second levellaboratory-based surveillance, strongly recommended)(Continued)

dressings,incontinentresidents withurinary or fecalcarriage, orresidents withtracheostomiesand difficulty inhandlingrespiratorysecretions

Selection ofLTCF residents

Perform activeCPE surveillancecultures (ormolecularmethods) on allresidents hostedin the sameLTCF unit as theindex case

Possibleextension ofsurveillancecultures to otherclose contacts ofthe index casein other LTCFunits; extensionof CPE-screeningto all residentsof the LTCF canbe considered,in agreementwith the infec-tion controlpractitioners inthe involvedLTCFs

LTCF physicians,LTCF infectionpreventionists,clinicalmicrobiologists

Specimen types Use rectal orfecal swabs forCPE-screening

Add otherspecificspecimen typesfor possiblescreening ofother MDROs

LTCF physicians,LTCF infectionpreventionists,clinicalmicrobiologists

Frequency ofsurveillance

Repeat CPEsurveillancecultures (ormolecularscreening) asrecommendedby the infectioncontrolprofessionals ofthe LTCF

Discussfrequency ofpossiblesurveillance forother MDROswith LTCFinfectionpreventionists

LTCF infectionpreventionists,clinicalmicrobiologists

Environmental orstaff screening

Do not performroutineenvironmentalcultures orscreeningcultures fromasymptomaticpersonnel

Discuss possibleextension ofscreening toenvironmentalsamples orasymptomaticpersonnel(generally notrecommended)with infectionpreventionists,clinicalmicrobiologists,epidemiologistsand infectiousdiseasespecialists

LTCF infectionpreventionists,infectiousdiseasespecialists,clinicalmicrobiologists,epidemiologists,

Data elaboration Integrate activeMDRO cultural

If possible,stratify screening

Clinicalmicrobiologists,

Surveillance by active surveillance cultures (second levellaboratory-based surveillance, strongly recommended)(Continued)

or molecularscreening datafrom LTCFresidents into ageneralantimicrobialsusceptibilitydata report,comparingscreening datafrom LTCFresidents withthose fromreferral ACHpatients

data from LTCFresidents,admitted within48 h to thereferral ACH,together withLTCF screeningdata

epidemiologists,

Isolateconservation

CryopreserveCPE-isolates (at− 80 °C)

Preserve forfurthermolecularcharacterization,in collaborationwith a referencemolecularbiologylaboratory

Clinicalmicrobiologists

Prospective MDRO surveillance surveys (thirdlevel laboratory-based surveillance, on avoluntary basis)Analysis of routine isolates from clinical diagnostic oractive screening cultures obtained from LTCF residentsis easy and cheap to perform, but the generally lownumber of routine clinical samples sent to themicrobiology laboratory for analysis limits the value ofthis strategy; nevertheless, it is generally difficult toinclude isolates from LTCF residents admitted to theacute care referral hospital in the LTCF surveillancereport. Moreover, with respect to the currentepidemiological situation of CPE in Italy, the presentrecommendations for active surveillance screening arefocused on CPE. Therefore, prospective surveillancesurveys, mainly based on point prevalence colonizationstudies are recommended, allowing to determine thebaseline prevalence of various MDROs in the facility;repeating of the active surveillance can then be used toevaluate the success of an intervention that wasimplemented in response to high MDRO-rates. We rec-ommend selecting highest prevalence LTCFs for inclu-sion in the prospective surveillance study, allowing toobtain a “worst case scenario” for a specific healthcareregion. Prospective surveillance can be limited to a resi-dent subgroup or may be facility-wide. We recommendperforming local, regional and national surveys to delin-eate the extent of MDRO colonization and infection inresidents of LTCFs. For culture based or molecularscreening of MDROs, microbiology methods routinely

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used in the referring microbiology laboratory can be ap-plied. Prospective surveys for MDROs based on cultur-ing specimens from clinically suspected infections canalso give significant laboratory-based surveillance results[17].Molecular typing of the associated isolates is important

for identification of resistance plasmids and of hyper-epidemic clonal groups [34], and may be helpful in asses-sing whether resident-to-resident transmission has oc-curred. Genotyping can utilize various methods, such aspulsed-field gel electrophoresis (PFGE) [12, 13, 35],polymerase chain reaction and sequence based methods[12, 15, 36], multi locus sequence typing (MLST) [15], upto whole-genome sequencing (WGS) [37], which is rapidlybecoming the new standard for the molecularcharacterization of isolates.We recommend prospective third level laboratory-

based surveillance as follows.

Theme of therecommendation

Recommendedstrategies

Comments Specificresponsibilities

Preparation ofsurveillanceproject

Prepare asurveillancesurvey project,in collaborationwith the LCTFphysicians andthe infectioncontrolpractitioners, tothe LTCFadministrationand the referralethicscommittee, thatincludesinstitutionalreview boardapproval for thesurvey

Consent fromresidents (ortheir legalrepresentatives)to participate isrequired

LTCFadministration,LTCF physicians,LTCF infectionpreventionists,clinicalmicrobiologists,epidemiologists,local ethicscommittee

LTCF selection Select at leastonerepresentativeLTCF in ahealthcaredistrict forperforming apoint prevalencescreeningsurvey, to obtainbaseline MDROcolonizationdata

Selection shouldbe done by thebodyoversighting thesurveillance.Preferably selectLTCFs with highprevalence ofMDROs (asderived fromroutine clinicaland/orscreening data)

LTCF physicians,infection controlpractitioners,clinicalmicrobiologists,epidemiologists

MDRO types Include at leastESBL- andcarbapenemase-producing Enter-obacterales,carbapenemase-producing A.baumannii,carbapenem-resistant P.

Possibleextension toother MDROs

Infection controlpractitioners,clinicalmicrobiologists,epidemiologists

Prospective MDRO surveillance surveys (third levellaboratory-based surveillance, on a voluntary basis)(Continued)

aeruginosa,MRSA and VRE

Specimen types Collect fromeach LTCFresident at leasta rectal (orfecal), anoropharyngeal(or nasal) andinguinal (orperineal) swab

Specimen typesrecommendedfor screening ofESBL- andcarbapenemase-producing Enter-obacterales andfor screening ofVRE are rectal orfecal swabs(possibly com-bined with urinesamples), forcarbapenem-resistant P. aeru-ginosa and A.baumannii werecommend rec-tal and oropha-ryngeal swabs(possibly com-bined with urinesamples), andfor MRSA werecommend acombination oforopharyngeal(or nasal) andinguinal (or peri-neal) swabs (to-gether withswabs fromwounds, ifpresent)

Infection controlpractitioners,clinicalmicrobiologists,epidemiologists

Frequency ofsurveillanceproject

Repeatsurveillancecultures in thesame LTCF atleast in a four-year interval

Shorter intervalsare preferred

Infection controlpractitioners,clinicalmicrobiologists,epidemiologists

Staff screening Performscreeningcultures fromasymptomaticpersonnel only ifstaff membersagree toparticipate inthe screeningstudy

Anonymous andonly forepidemiologicdata collection

Infection controlpractitioners,LTCF personnel,clinicalmicrobiologists,epidemiologists

Isolateconservation

CryopreserveMDR-isolates (at−80 °C)

Preserve forfurthermolecularcharacterization,in collaborationwith a referencemolecularbiologylaboratory

Clinicalmicrobiologists

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Infection control measuresLaboratory-based surveillance of MDROs is onlyeffective if the collected data are used by healthcareprofessionals [38]:

� to better address empiric therapy of infectiousdiseases

� to guide infection control activities (e.g. isolationprecautions for residents to prevent transmission)

� to plan educational programs� to identify trends in resistance� to detect outbreaks requiring prompt therapeutic

and infection control actions

Exhaustive guidelines providing basic information forinfection prevention and control in LTCFs have beenpublished by the Society for Healthcare Epidemiology ofAmerica (SHEA) in collaboration with the Associationfor Professionals in Infection Control (APIC) and by theRoyal College of Physicians Clinical Advisory Group onHealthcare Associated Infections [1, 2, 39]. Guidelinesagree that for the control of MDROs in LTCFs, besideshygiene measures, the implementation of antimicrobialstewardship programs is pivotal for the improvement ofantibiotic use [3].Finally, any discussion of MDRO control issues in

LTCFs must be made in the context of these facilities asa home for residents, in which they usually reside formonths or years, and therefore the resident’s livingcomfort must be addressed together with the control ofMDROs. In the absence of risk factors for sheddinglarge numbers of MDROs, LTCF residents should not berestricted from participation in social or therapeuticgroup activities within the facility, unless there is reasonto think that they have been implicated in thedevelopment of infections in other residents [2].

Summary and conclusionsRoutine surveillance of MDROs in LTCFs needs to besimple, pragmatic and sustainable. Laboratory-basedroutine testing of isolates from cultures taken for “clin-ical” purposes is the most cost-effective and less labor-intensive method to track MDROs. Therefore, wepropose this method as mandatory first level laboratory-based MDRO surveillance strategy in Italian LTCFs.On the other hand, active surveillance cultures (or

PCR based methods) report asymptomatic colonizationby MDROs (e.g., rectal swabs for CPE). Laboratory-based active screening results may complement routinediagnostic data, and are strongly recommended when anLTCF reports a case of infection by CPE (second levellaboratory-based MDRO-screening).

Prospective surveillance surveys for various MDROs(third level laboratory-based MDRO-screening), basedon prospective culturing of specimens from clinicallysuspected infections, and especially on point prevalencestudies, is costly and time-consuming, but yields themost significant laboratory-based surveillance results; es-pecially if isolates are molecularly characterized andgenotyped.We therefore recommend a stepwise application of the

three MDROs surveillance levels, initially focusing onthe elaboration of data from diagnostic bacterial isolates,in a second step extending this procedure to activesurveillance screening for CPE, and finally performingprospective point prevalence studies in selected LTCFs.Finally, it is mandatory that the collected and elaboratedMDROs surveillance data be used by healthcareprofessionals to inform decisions for infectionprevention and control strategies, targeting the uniqueaspects of LTCFs.

AbbreviationsGLISTer: Gruppo di Lavoro per lo studio delle Infezioni nelle ResidenzeSanitarie Assistite e Strutture Territoriali Assimilabili (Italian working group forthe study of infections in LTCFs); AMCLI: Associazione Microbiologi CliniciItaliani (Italian Association of Clinical Microbiologists); LTCF: Long-term carefacility: encompass nursing homes, residential care centers, chronic diseasehospitals, rehabilitation centers and institutions for mentally handicappedpersons; MDRO: Multidrug-resistant organism: methicillin-resistant Staphylo-coccus aureus (MRSA), vancomycin-resistant enterococci (VRE), Pseudomonasaeruginosa or Acinetobacter baumannii with MDR phenotype (resistance to≥3 classes of antibiotics), Enterobacterales producing extended-spectrum β-lactamases (ESBL), high-level cephalosporinases (AmpCs) and/or carbapene-mases; PNCAR 2017–20: Piano Nazionale di Contrasto dell’Antimicrobico-Resistenza 2017–20 (Italian plan for contrasting of antimicrobial resistance2017–20)

AcknowledgementsThese recommendations were prepared and approved by the GLISTerWorking Group of AMCLI and do not necessarily reflect the opinions ofAntimicrobial Resistance and Infection Control or its Editors.Members of the GLISTer working group: Massimo Confalonieri (Piacenza),Claudio Farina (Bergamo), Paolo Fazii (Pescara), Francesco Luzzaro (Lecco),Roberto Rigoli (Treviso), Melissa Spalla (Pavia).

Authors’ contributionsRA conceived the study, participated in its design and coordination anddrafted the manuscript; LP participated in the study design, providedtechnical improvement, and drafted the manuscript; RM participated in thestudy design and coordination and drafted the manuscript; LP conceived thestudy, coordinated and led its different parts and reviewed the manuscript.The authors read and approved the final manuscript.

FundingNo source of funding to declare.

Availability of data and materialsData sharing not applicable to this article as no datasets were generated oranalyzed during the current study.

Ethics approval and consent to participateNot applicable.

Consent for publicationNot applicable.

Aschbacher et al. Antimicrobial Resistance and Infection Control (2020) 9:106 Page 10 of 12

Competing interestsThe authors declare that they have no competing interests.

Author details1Microbiology and Virology Laboratory, Bolzano Central Hospital, Bolzano,Italy. 2Infectious Diseases Unit, Bolzano Central Hospital, Bolzano, Italy.3Department of Clinical-Surgical, Diagnostic and Pediatric Sciences, Unit ofMicrobiology and Clinical Microbiology, University of Pavia, Pavia, Italy.

Received: 2 January 2020 Accepted: 2 July 2020

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