Research Article Extended Spectrum Beta-Lactamase Carriage ...downloads.hindawi.com/journals/tswj/2015/987580.pdf · Research Article Extended Spectrum Beta-Lactamase Carriage State

Research ArticleExtended Spectrum Beta-Lactamase Carriage State amongElderly Nursing Home Residents in Beirut

M A Jallad1 R Naoufal2 J Irani2 and E Azar2

1Faculty of Medicine American University of Beirut Beirut Lebanon2Faculty of Medicine and Medical Sciences University of Balamand Beirut Lebanon

Correspondence should be addressed to M A Jallad maryannjalladgmailcom

Received 5 October 2014 Revised 25 January 2015 Accepted 25 February 2015

Academic Editor John Stelling

Copyright copy 2015 M A Jallad et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Introduction ESBL-producing Enterobacteriaceae can cause severe infections but they are also isolated from the stool ofasymptomatic subjects Faecal carriage of such organism is poorly understoodMethods First phase of the study was cross-sectionalwith prevalence and epidemiology of ESBL faecal carriage in two nursing homes in Beirut 57 residents in the first (NH1) and 151residents in the second (NH2) In second phase faecal swabs from cohort of NH1 residents were examined for carriage at six-week intervals over three-month period Residentsrsquo charts were reviewed to assess carriage risk factors ResultsOver 3 consecutivesamplings at NH1 81 of residents were at least one-time carriers with 50 at the first round 604 at the second and 745 atthe last one At NH2 682 of residents were carriers Constipation (in NH1) and antibiotic intake (in NH2) were significantlyassociated with higher ESBL faecal carriage while the length of stay at the nursing home (in NH2) was associated with less carriageConclusion Faecal carriage of ESBL-producing Enterobacteriaceae is high among nursing home patients in Beirut The rate ofcarriage changes rapidly and significantly over time either with multiple factors playing a possible role like outbreak spreadingantibiotic and health care system exposure

1 Introduction

Beta-lactam antibiotics are extensively used in the treatmentof several types of infections [1ndash3] Extended spectrum beta-lactamases (ESBLs) are enzymes produced by bacteria andcapable of hydrolysing beta-lactam antibiotics [4 5]The firstESBLs were identified in the 1980s Point mutations at thelevel of the beta-lactamase active site transformed parentnon-ESBL TEM-1 TEM-2 and SHV-1 into ESBL TEM andSHV Throughout the 1980s and 1990s the main types ofESBLs were TEM and SHV and were mostly produced byKlebsiellaThey weremainly isolated in hospital settings fromnosocomial infections However from the year 2000 a wholeshift in the epidemiology took place [6] ESBLs were alsoproduced by E coli strains and were increasingly isolatedin community settings The main ESBLs became CTX-Mtype [6] This new type of ESBL is thought to originatefrom a bacterial species in the environment Kluyvera [6 7]While most ESBL-producing strains were clonally related inthe past the newer CTX-M-type ESBLs producing bacteria

were not [8] ESBL-producing strains are being increasinglyisolated throughout time This can be explained by theeasy transmission of CTX-M encoding plasmids throughconjugation [9]

In Lebanon the genes blaCTX-M blaTEM and blaSHV wereall found in clinical isolates of ESBL-producing E coli andKlebsiella spp In addition a 90 kb plasmid was identified[10] This plasmid can transmit ESBL resistance as well asresistance to quinolones across bacteria since it harboursgenes encoding CTX-M15 and AAC(61015840)-Ib-cr which is aquinolone-modifying enzyme [10]

Studies done in Lebanese hospitals showed a constantrise in prevalence of ESBL-producing strains [11] Statisticsfrom the Saint Georges Hospital University Medical Centrein Beirut showed that in 1998 33 of E coli and 64 ofKlebsiella strains were ESBL producers (unpublished data)While in 2011 34 of E coli and 72 of Klebsiella strains(isolated from urine) were ESBL producers

With such high prevalence ESBL-producing bacteriabecame the subject of concern of many researchers owing to

Hindawi Publishing Corporatione Scientific World JournalVolume 2015 Article ID 987580 7 pageshttpdxdoiorg1011552015987580

2 The Scientific World Journal

two major points The first point is the hurdle of treatment ofinfections caused by these pathogens with powerful antibi-otics which often necessitates hospitalisation The secondpoint is the frequent transferability of this resistance amongbacteria resulting in increasing rates of ESBL infections andcarriageThemeans of acquiring ESBL are not yet completelyunderstood with several gaps remaining as to the spreadof this resistance in the community and among health carefacilities residents Moreover ESBL strains are being isolatedin nursing homes and other health care associated facilitiesin the community [12ndash18] This suggests the presence of areservoir for these resistant strains outside hospital wards

This study seeks to estimate the prevalence of ESBL faecalcarriage among nursing home residents in Beirut and howthis prevalence varies with time In addition this study is anattempt to give insight into the characteristics of ESBL faecalcarriers and the risk factors associated with this carriageamong nursing home residents

2 Materials and Methods

21 Study Design We conducted a cross-sectional study attwo different nursing homes in Beirut In one of the nursinghomes we followed a cohort of patients prospectively inorder to determine the change in carriage status and thedevelopment of UTI

22 Population The data was collected at the Saint GeorgesHospital Nursing Home (NH1) and the Dar Al-Ajaza Al-Islamia Nursing Home (NH2) NH1 included 30 rooms andhad a capacity of 70 beds NH2 had an 800-bed capacityincluding 400 beds for psychiatry andmental retardation and400 beds for the elderly All the individuals who were nursinghome residents andwhowere above the age of 65were eligiblefor the study Individuals who (or whose surrogate) refused tosign the consent formwere excluded Candidateswhomet theinclusion criteria were systematically included All residentsof NH1 were eligible and signed the consent form Rectalswabbingwas repeated three times among these residents thefirst was in April 2012 (119879

0) the second was in May 2012 (119879

1)

and the third was in July 2012 (1198792)

23 Procedure The faecal carriage was determined by per-forming rectal swabbing on all participants Rectal swabbingwas performed since the sensitivity and specificity of thistechnique were proved to be to a great extent higher thanthose of stool samples in determining faecal carriage [15]The swabs were then cultured on specific chromogenic agarmedia (ChromID ESBL Biomerieux Marcy lrsquoEtoile France)ESBL detection was done according to CLSI guidelinesusing disk diffusion test for cefotaxime and ceftazidimealong with amoxicillin-clavulanic acid [19] for detection ofsynergy (keyhole effect) in a double disk synergy methodPossible Amp C resistance was detected by cefoxitin disksCiprofloxacin disks were used to test for quinolone resistanceThe identification of all the strains was done using API20E kit (Biomerieux France) Finally all isolated strains

were preserved in a ltndash80∘C freezer in cupules containing acombination of nutrient broth (85) and glycerol (15)

The medical records of all participants were checkedat the beginning of the study A questionnaire was usedto gather details about patientsrsquo age gender length of stay(LOS) at the nursing home diagnosis on admission mobilitystatus comorbidities (neurologic diseases diabetes cancercardiovascular diseases pulmonary diseases and under-lying urogenital pathologies) bladderbowel incontinenceindwelling medical devices (permanent and intermittenturinary catheters) and hospital admissions during the lastyear and antibiotic treatments in the preceding 3 monthsAt NH1 the faecal carriage was reexamined and the medicalrecords were reviewed every 6 weeks to note any alterationin the medical condition A case of ESBL faecal carriagewas defined as an individual who had at least one positivecarriage All NH1 participants were monitored for the onsetof any UTI to examine whether it was an infection with anESBL-producing strain A UTI is an infection involving anypart of the urinary system including urethra bladder uretersprostate and kidneys A case definition of a UTI consists ofclinical (dysuria urgency frequency suprapubic tendernessand flank pain) and microbiological (pure culture of a singlemicroorganism and a colony count higher than 105 colonyforming units per mL) findings

24 Statistics and Data Analysis Classical descriptive meth-ods were used for univariate analysis for the whole sampleand according to the study site Continuous variables (agelength of stay) were described using means medians andstandard deviations Categorical data were summarized usingproportions Additionally bivariate analysis was performedto compare different variables according to the carriagestatus Quantitative data were compared using Studentrsquos 119905-testor Mann-Whitney 119880 test when appropriate Qualitative datawere compared using Chi-square or Fisherrsquos exact test whenappropriate Analysis was performed for each site alone 119875values below 005 were considered statistically significant Noadjustment formultiple comparisonswasmade All statisticalcalculations were performed using SPSS V20 (IBM SPSSStatistics 200)

3 Results

31 Prevalence and Dynamics of ESBL Faecal Carriage Theoverall number of individuals included in the study at leastonce during the 3 phases at NH1 was 57 At NH2 a one-timerectal swabbing took place in August 2012 and 151 residents(755 of eligible individuals) signed the consent form Theparticipantsrsquo demographic and medical data are presented inTable 1 In NH1 at 119879

0 26 of 52 residents (50) were positive

for ESBL faecal carriage At 1198791 32 of 53 residents (604)

were positive Finally at 1198792 38 of 51 residents (745) were

positive Overall 46 of 57 individuals (807) were at leastone-time carriers during the follow-up time while only 11 of57 individuals (193)were never carriers Between119879

0and1198791

the ESBL faecal carriage disappeared in 5 residents (102)while 9 residents (184) acquired this carriage Between 119879

1

The Scientific World Journal 3

Table 1 Characteristics of the participants from NH1 and NH21

NH1 NH2Total number 57 151Gender

Male 19 (333) 54 (358)Female 38 (667) 97 (642)

Age (years) mean (plusmnSD) 848 (plusmn53) 779 (plusmn79)LOS (months) median(interquartile range) 25 (285) 32 (60)

Room accommodationSingle 13 (228) 10 (66)Double 19 (333) 4 (26)Triple 9 (158) 54 (358)Quadruple 16 (281) 1 (07)More than 4 bedsroom None 82 (543)

History of UTI (in the prior 12months) 16 (281) 8 (53)

Non-ESBL UTI (in the prior 12months) 14 (246) sect

ESBL UTI (in the prior 12months) 7 (123) sect

History of hospitalization duringthe prior 12 months 28 (492) 4 (26)

History of antibiotic use duringthe prior 3 months 29 (508) 23 (152)

ComorbiditiesCardiovascular 45 (789) sectPulmonary 6 (105) sectDiabetes mellitus 12 (211) sectNeurologic 26 (456) sectRenal 7 (123) sectCancer 3 (53) sectUrogenital pathology 24 (421) sect

1All the data presented in the table is by number () unless stated otherwisesectData unavailable

and 1198792 the carriage disappeared in 3 residents (6) while it

was acquired by 10 residents (20) At NH2 the number ofESBL faecal carriers was 103 of 151 participants (682) InNH1 andNH2 combined 149 of 208 participants (716)werecarriers

Figure 1 summarises the prevalence of the carriage andFigure 2 shows its dynamics between the different samplingtimes

32 Characterisation of the Isolated Strains Some positivecarriers had more than one bacterial strain producing ESBL(up to 4 strains) In total 226 strains were isolated andpreserved and were distributed as follows 187 E coli (827)22Klebsiella (97) 9 Enterobacter (4) 4Citrobacter (18)3 Proteus (13) and 1 Serratia (05) On average out of 199positive samples 75 samples had resistance to ciprofloxacin(38) and 29 samples had at least one strain resistant tocefoxitin (15) hence a possible AmpC resistance

506040

74506821 716

0

10

20

30

40

50

60

70

80

()

NH1 at T0 NH1 at T1 NH1 at T2 NH2 NH1 + NH2

Prevalence ()

Figure 1 Percentages of prevalence of ESBL faecal carriage

1020

6

1840 20

000

500

1000

1500

2000

2500

()

Between T0 and T1 Between T1 and T2

ESBL disappearance ()ESBL appearance ()

Figure 2 Dynamics of the ESBL faecal carriage at NH1

33 Incidence of UTI Throughout the period of the 3 con-secutive samplings at NH1 9 individuals developed a UTI(158) 5 of which were caused by non-ESBL-producingstrain (88) while 4 were caused by ESBL-producing strain(7)

34 Risk Factors for ESBL Faecal Carriage The associationbetween different factors and the ESBL faecal carriage at NH1and NH2 is presented in Table 2 As for NH1 a statisticallysignificant association was noted between constipation andESBL faecal carriage (119875 value of 0049) The constipatedindividuals were 100 carriers while the nonconstipatedare 744 carriers Moreover the chart review of the NH1residents showed that 15 of the 51 residents (29) usedquinolones in the 3 months prior to the first sampling 5out of the 53 residents (94) were exposed between samplesone and two but only 3 out of the 51 subjects (58)were prescribed quinolones between the second and thirdsampling At NH2 statistical significance was found for theassociation between LOS and ESBL faecal carriage with a 119875value of 0007 Also at NH2 statistical significance was shownfor the association between any antibiotic intakes during thelast three months before the study with a 119875 value of 0036Residents who have an antibiotic intake are 87 carriers andthose with no antibiotic intake are 648 carriers


Table 2 Association between different factors and the ESBL faecal carriage at NH1 NH2 and both combined1

NH1 NH2Carrierslowast Noncarriers Carriers Noncarriers

Total number 46 (807) 11 (193) 103 (682) 48 (318)Male 16 (348) 3 (273) 36 (35) 18 (375)

Age (years) mean (plusmnSD) 843 (plusmn52) 874 (plusmn52) 784 (plusmn75) 772 (plusmn87)LOS (months) median (interquartile range) 24 (288) 25 (32) 32 (48)

daggerb50 (117)

daggerb

Room accommodationSingle 10 (217) 3 (273) 8 (78) 2 (42)Double 16 (348) 3 (273) 3 (29) 1 (21)Three or more 20 (435) 5 (454) 92 (893) 45 (937)

Patient characteristicsUrinary continent 14 (304) 1 (91) 27 (262) 12 (25)Bowel continent 16 (348) 1 (91) 29 (282) 13 (271)Suffering from constipation 14 (304)

daggera0 (0)daggera 3 (29) 1 (21)

Bedridden or in wheelchair 11 (239) 6 (545) Dagger Dagger

History of UTIAbsent 22 (478) 4 (364) 97 (942) 46 (958)Less than twice in 6 months 9 (196) 3 (272) 4 (39) 1 (21)More than twice in 6 months 15 (326) 4 (364) 2 (19) 1 (21)

Hospitalized during the prior 12 monthsDagger 14 (56) 10 (385) 4 (39) 0With any antibiotic intake within the prior 3 monthsDagger 14 (538) 12 (461) 20 (194)

daggerc3 (63)

daggerc

1All the data presented in the table is by number ( within dependent variable) unless stated otherwiselowastNH1 data is based on the case definition of the faecal carriage that is being at least 1-time carrier through follow-updaggerA statistically significant difference (119875 value lt005) between the ESBL carrier and ESBL noncarrier cases was identified (a119875 = 0049 b119875 = 0007 and c

119875 =

0036)DaggerData unavailable

4 Discussion

There has been little published data from Lebanon lookinginto the prevalence of ESBL faecal carriage a study byMoubareck et al [20] inspected the carriage in ICU patientsfrom 5 hospitals 58 healthcare workers and 382 healthysubjects in the year 2003 The prevalence showed 16carriage in ICU patients 34 in health care workers and24 in healthy subjects

Prevalence in long-term care facilities and NHs innonoutbreak settings varied significantly from 19 inFrance [17877 2012] [21] to 64 in Italy [71111 2009] [15]and 405 in UK [119294 2009] [14] The particularly lowprevalence in France can be attributed to poor screeningmethod as stated in the study itself Another study in France[22] showed that prevalence in asymptomatic young adultsgrew from0 in 1999 to 21 in 2009The prevalence of ESBLfaecal carriage among healthy individuals fluctuated betweencountries in Egypt 63 [400632 2011] [23] in Spain 67[7105 2009] [18] in Saudi Arabia 123 [62505 2009] [17]in China 7 of elderly people [19270 2008] [16] and inThailand 518 [73141 2010] [24] The carriage rate wasaffected by exposure to health care system In the Republic ofKorea for instance prevalence in elderly healthy individualswas 23 [939 2012] while prevalence in hospitalised indi-viduals of the same age group was 491 [2857 2012] [25]In Cameroon as well prevalence in student volunteers was67 [10150 2012] while prevalence in outpatients was 231[48208 2012] [26]

In our study a high incidence of detection ESBL-producing Enterobacteriaceae was detected at both nurs-ing homes At NH1 the prevalence was 50 with 73of the isolates ciprofloxacin resistant at the first samplingThe prevalence increased to 604 six weeks later butciprofloxacin resistance decreased to 44 On our last sam-pling the proportion of residents carrying ESBL in their stoolincreased to 745 but a minority of 27 continued to beciprofloxacin resistant Assuming that therewere no technicaland sampling variations this rise may well be the resultof an outbreak with an ESBL-producing but ciprofloxacinsensitive organism at the concerned NH The consumptionof quinolones decreased markedly from 29 in the 3 monthsprior to the first sampling to 94 in the first 6 weeks ofstudy and to 58 in the last 6 weeks this may have affectedthe profile of resistance to ciprofloxacin in ESBL-producingstrains but the small numbers are not enough to confirm sucha conclusion The distribution of strains found in our studyis similar to that in the literature Studies inspecting rectalcolonisation with ESBL-producing strains as well as studiesexamining the isolation of such strains from clinical samplesshow a similar strain distribution [11 15 17 19 23 27]

During the 3-month follow-up time of the study at NH19 residents (158) developed a urinary tract infection 4were due to ESBL-producing strains and 5 due to non-ESBL-producing organisms All 4 participants who had UTIwith ESBL-producing organismswere females their infectionwas mild and they did not require hospitalisation for their


infection or any other reason during the study time Twosubjects were carriers during the 3 samplings the othertwo were carriers before the development of their infectionbut that carriage disappeared on further follow-ups Therelation between carriage and infection has been validatedin multiple studies [5 9 28ndash30] though our small sampleprevents us fromfirm conclusions in that regard In a study byDaoud and Afif [31] assessing all UTIs of both inpatients andoutpatients at our university medical centre Saint GeorgesHospital from year 2000 till year 2009 a considerable riseis shown in ESBL prevalence from 23 in 2000 to 168in 2009 The proportion of urinary tract infections due toESBL E coli strains rose exponentially from 2000 till 2006and then stabilised at 192 out of 688 isolates in 2007171 out of 727 isolates in 2008 and finally 168 out of628 in 2009 The great variability in the faecal carriage ofESBL-producing organisms and their ciprofloxacin resistanceprofile contrasted with a fairly steady burden of disease dueto ESBL-producing organisms in urinary tract infection inaddition the known complexity of the intestinal microbiotamay lead us to consider faecal carriage as dynamic withacquisition loss and coexistence of multiple strains Sucha conclusion will need to be verified in a large prospectivecohort study on populations from different areas in Lebanonover a longer period of time

NH1 andNH2 are both situated in BeirutThey are similarinmean age of residents and gender distribution but differentin median stay room accommodations and hospitalisationscheme and antibiotics intake (Table 1) Therefore the data ofeach nursing home was analysed separately Characteristicsassociated with ESBL faecal carriage in elderly nursing homeresidents in Beirut (Table 2) were constipation in NH1antibiotic intake in the last 3 months in NH2 and lengthof stay in the nursing home in NH2 There is no publishedcorrelation between constipation and faecal carriage butconstipation is a known risk factor for development of UTIsthat subsequently can affect the faecal carriage Exposure toany antibiotic in the 3 months prior to the faecal sampling isassociated with a higher detection of ESBL-producing organ-ism such association was demonstrated in many studies [14ndash16 21 32 33] Several studies identify quinolone intake andspecifically ciprofloxacin as a risk factor for the developmentor persistence of ESBL faecal carriage [12 26 34] Finallya longer length of stay at the nursing home was associatedwith a lower risk of carriage comparable findings werepreviously reported by Rooney et al [14] Twenty-five percentof newcomers were recently hospitalised as compared with128 of long-term residents (119875 value = 0046) A higherpercentage of antibiotic exposure was noted in the newcomerresidents (293) than in the formerly admitted (226) butdoes not reach significance (Figure 3) To note that antibioticconsumption was calculated based on patient reportingand nursing home charts this may have underestimatedthe intravenous antibiotherapy given during hospitalisationPatients with short nursing home staysmay be fundamentallydifferent from patients with long nursing home stays Forexample patients with short nursing home stays reflect amix of both patients with recent hospitalizations surgeriesor medical interventions with high antibiotic use and the

Hospitalisation Antibiotic intake

Recently admittedFormerly admitted

252930

1280

2260

0

5

10

15

20

25

30

35

()

Figure 3 Percentages of hospitalisation and antibiotic intake inrecently admitted residents versus formerly admitted residents

intention that most will go home in a short period of timeand elderly relatively healthy individuals who will eventuallygo on to become long-term nursing residents It is possiblethat this first group of patients may have transient or short-term ESBL carriage and thus only pose a risk to others in theshort term whereas it is possible that the long-term residentsmight be chronic carriers and thus pose a greater risk to thecommunity

In conclusion stool carriage with ESBL-producing Enter-obacteriaceae is high among nursing home residents playingpossibly a role in the endemic status of ESBL urinary tractinfection A higher carriage was noted in newcomers withrecent exposure to health care system and antibiotics Thesefindings are another good reason to conduct larger studieslooking into the dynamics and implications of fecal carriage

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] M H Abdul-Aziz J M Dulhunty R Bellomo J Lipman andJ A Roberts ldquoContinuous beta-lactam infusion in critically illpatients the clinical evidencerdquo Annals of Intensive Care vol 2no 1 article 37 2012

[2] R P Dellinger M M Levy J M Carlet et al ldquoSurviving sepsiscampaign international guidelines for management of severesepsis and septic shockrdquo Critical Care Medicine vol 36 no 1pp 296ndash327 2008

[3] J M Dulhunty D Paterson S A R Webb and J LipmanldquoAntimicrobial utilisation in 37 Australian and New Zealandintensive care unitsrdquoAnaesthesia and Intensive Care vol 39 no2 pp 231ndash237 2011

[4] J D D Pitout ldquoInfections with extended-spectrum beta-lactamase-producing enterobacteriaceae changing epidemiol-ogy and drug treatment choicesrdquo Drugs vol 70 no 3 pp 313ndash333 2010

[5] J OteoM Perez-Vazquez and J Campos ldquoExtended-spectrum120573-lactamase producing Escherichia coli changing epidemiologyand clinical impactrdquo Current Opinion in Infectious Diseases vol23 no 4 pp 320ndash326 2010


[6] M E Falagas andD E Karageorgopoulos ldquoExtended-spectrumbeta-lactamase-producing organismsrdquo Journal of Hospital Infec-tion vol 73 no 4 pp 345ndash354 2009

[7] Y Pfeifer A Cullik andWWitte ldquoResistance to cephalosporinsand carbapenems in Gram-negative bacterial pathogensrdquo Inter-national Journal ofMedicalMicrobiology vol 300 no 6 pp 371ndash379 2010

[8] R Ben-Ami J Rodrıguez-Bano H Arslan et al ldquoA multi-national survey of risk factors for infection with extended-spectrum 120573-lactamase-producing enterobacteriaceae in non-hospitalized patientsrdquo Clinical Infectious Diseases vol 49 no 5pp 682ndash690 2009

[9] R Ben-Ami M J Schwaber S Navon-Venezia et al ldquoInfluxof extended-spectrum beta-lactamase-producing enterobacte-riaceae into the hospitalrdquoClinical InfectiousDiseases vol 42 no7 pp 925ndash934 2006

[10] S S Kanj J E Corkill Z A Kanafani et al ldquoMolecular char-acterisation of extended-spectrum beta-lactamase-producingEscherichia coli and Klebsiella spp isolates at a tertiary-carecentre in Lebanonrdquo Clinical Microbiology and Infection vol 14no 5 pp 501ndash504 2008

[11] Z Daoud C Moubareck N Hakime and F Doucet-PopulaireldquoExtended spectrum 120573-lactamase producing enterobacteri-aceae in lebanese ICU patients epidemiology and patterns ofresistancerdquo Journal of General and AppliedMicrobiology vol 52no 3 pp 169ndash178 2006

[12] J Rodriguez-Bano and M D Navarro ldquoExtended-spectrumbeta-lactamases in ambulatory care a clinical perspectiverdquoClinical Microbiology and Infection vol 14 supplement 1 pp104ndash110 2008

[13] R Canton A Novais A Valverde et al ldquoPrevalence and spreadof extended-spectrum 120573-lactamase-producing Enterobacteri-aceae in Europerdquo Clinical Microbiology and Infection vol 14supplement 1 pp 144ndash153 2008

[14] P J Rooney M C OrsquoLeary A C Loughrey et al ldquoNursinghomes as a reservoir of extended-spectrum 120573-lactamase(ESBL)-producing ciprofloxacin-resistant Escherichia colirdquoJournal of Antimicrobial Chemotherapy vol 64 no 3 pp635ndash641 2009

[15] A March R Aschbacher H Dhanji et al ldquoColonization ofresidents and staff of a long-term-care facility and adjacentacute-care hospital geriatric unit by multiresistant bacteriardquoClinical Microbiology and Infection vol 16 no 7 pp 934ndash9442010

[16] S F Tian B Y Chen Y Z Chu and S Wang ldquoPrevalence ofrectal carriage of extended-spectrum 120573-lactamase- producingEscherichia coli among elderly people in community settings inChinardquoCanadian Journal ofMicrobiology vol 54 no 9 pp 781ndash785 2008

[17] A A Kader and K A Kamath ldquoFaecal carriage of extended-spectrum beta-lactamase-producing bacteria in the commu-nityrdquo Eastern Mediterranean Health Journal vol 15 no 6 pp1365ndash1370 2009

[18] L Vinue Y Saenz S Martınez et al ldquoPrevalence and diversityof extended-spectrum 120573-lactamases in faecal Escherichia coliisolates from healthy humans in Spainrdquo Clinical Microbiologyand Infection vol 15 no 10 pp 954ndash956 2009

[19] J D Pitout and K B Laupland ldquoExtended-spectrum beta-lactamase-producing Enterobacteriaceae an emerging public-health concernrdquoThe Lancet Infectious Diseases vol 8 no 3 pp159ndash166 2008

[20] C Moubareck Z Daoud N I Hakime et al ldquoCountry-wide spread of community- and hospital-acquired extended-spectrum beta-lactamase (CTX-M-15)-producing Enterobacte-riaceae in Lebanonrdquo Journal of ClinicalMicrobiology vol 43 no7 pp 3309ndash3313 2005

[21] X Bertrand M Amara M Sauget et al ldquoExtended-spectrumbeta-lactamase-producing Enterobacteriacae unexpected lowprevalence of carriage in elderly French residentsrdquo Age andAgeing vol 41 no 2 Article ID afr173 pp 233ndash237 2012

[22] F Janvier A Merens D Delaune C Soler and J-D CavalloldquoFecal carriage of third generation cephalosporins resistantenterobacteteriaceae in asymptomatic young adults evolutionbetween 1999 and 2009rdquo Pathologie Biologie vol 59 no 2 pp97ndash101 2011

[23] E M Abdul Rahman and R H El-Sherif ldquoHigh rates of intesti-nal colonization with extended-spectrum lactamase-producingEnterobacteriaceae among healthy individualsrdquo Journal ofInvestigative Medicine vol 59 no 8 pp 1284ndash1286 2011

[24] T Sasaki I Hirai M Niki et al ldquoHigh prevalence of CTX-M120573-lactamase-producing enterobacteriaceae in stool specimensobtained from healthy individuals in Thailandrdquo Journal ofAntimicrobial Chemotherapy vol 65 no 4 pp 666ndash668 2010

[25] Y J Ko H-W Moon M Hur C M Park S E Cho and YM Yun ldquoFecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in Korean community and hos-pital settingsrdquo Infection vol 41 no 1 pp 9ndash13 2013

[26] C M Lonchel C Meex J Gangoue-Pieboji et al ldquoProportionof extended-spectrum szlig-lactamase-producing Enterobacteri-aceae in community setting in Ngaoundere Cameroonrdquo BMCInfectious Diseases vol 12 article 53 2012

[27] P Herindrainy F Randrianirina R Ratovoson et al ldquoRec-tal carriage of extended-spectrum beta-lactamase-producingGram-negative bacilli in community settings in MadagascarrdquoPLoS ONE vol 6 no 7 Article ID e22738 2011

[28] R Friedmann D Raveh E Zartzer et al ldquoProspective eval-uation of colonization with extended-spectrum 120573-lactamase(ESBL)-producing enterobacteriaceae among patients at hos-pital admission and of subsequent colonization with ESBL-producing enterobacteriaceae among patients during hospital-izationrdquo InfectionControl andHospital Epidemiology vol 30 no6 pp 534ndash542 2009

[29] M J DiNubile I R Friedland C Y Chan et al ldquoBowel col-onization with vancomycin-resistant enterococci after antimi-crobial therapy for intra-abdominal infections observationsfrom 2 randomized comparative clinical trials of ertapenemtherapyrdquo Diagnostic Microbiology amp Infectious Disease vol 58no 4 pp 491ndash494 2007

[30] D Schoevaerdts P Bogaerts A Grimmelprez et al ldquoClini-cal profiles of patients colonized or infected with extended-spectrum beta-lactamase producing Enterobacteriaceae iso-lates a 20 month retrospective study at a Belgian UniversityHospitalrdquo BMC Infectious Diseases vol 11 article 12 2011

[31] Z Daoud and C Afif ldquoEscherichia coli isolated from uri-nary tract infections of Lebanese patients between 2000 and2009 epidemiology and profiles of resistancerdquo ChemotherapyResearch and Practice vol 2011 Article ID 218431 6 pages 2011

[32] E Ruppe A Pitsch F Tubach et al ldquoClinical predictive val-ues of extended-spectrum beta-lactamase carriage in patientsadmitted tomedical wardsrdquo European Journal of Clinical Micro-biology and Infectious Diseases vol 31 no 3 pp 319ndash325 2012

[33] S Fircanis and M McKay ldquoRecognition and managementof extended spectrum beta lactamase producing organisms


(ESBL)rdquo Medicine and Health Rhode Island vol 93 no 5 pp161ndash162 2010

[34] J Oteo C Navarro E Cercenado et al ldquoSpread of Escherichiacoli strains with high-level cefotaxime and ceftazidime resis-tance between the community long-term care facilities andhospital institutionsrdquo Journal of Clinical Microbiology vol 44no 7 pp 2359ndash2366 2006

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two major points The first point is the hurdle of treatment ofinfections caused by these pathogens with powerful antibi-otics which often necessitates hospitalisation The secondpoint is the frequent transferability of this resistance amongbacteria resulting in increasing rates of ESBL infections andcarriageThemeans of acquiring ESBL are not yet completelyunderstood with several gaps remaining as to the spreadof this resistance in the community and among health carefacilities residents Moreover ESBL strains are being isolatedin nursing homes and other health care associated facilitiesin the community [12ndash18] This suggests the presence of areservoir for these resistant strains outside hospital wards

This study seeks to estimate the prevalence of ESBL faecalcarriage among nursing home residents in Beirut and howthis prevalence varies with time In addition this study is anattempt to give insight into the characteristics of ESBL faecalcarriers and the risk factors associated with this carriageamong nursing home residents

2 Materials and Methods

21 Study Design We conducted a cross-sectional study attwo different nursing homes in Beirut In one of the nursinghomes we followed a cohort of patients prospectively inorder to determine the change in carriage status and thedevelopment of UTI

22 Population The data was collected at the Saint GeorgesHospital Nursing Home (NH1) and the Dar Al-Ajaza Al-Islamia Nursing Home (NH2) NH1 included 30 rooms andhad a capacity of 70 beds NH2 had an 800-bed capacityincluding 400 beds for psychiatry andmental retardation and400 beds for the elderly All the individuals who were nursinghome residents andwhowere above the age of 65were eligiblefor the study Individuals who (or whose surrogate) refused tosign the consent formwere excluded Candidateswhomet theinclusion criteria were systematically included All residentsof NH1 were eligible and signed the consent form Rectalswabbingwas repeated three times among these residents thefirst was in April 2012 (119879

0) the second was in May 2012 (119879

1)

and the third was in July 2012 (1198792)

23 Procedure The faecal carriage was determined by per-forming rectal swabbing on all participants Rectal swabbingwas performed since the sensitivity and specificity of thistechnique were proved to be to a great extent higher thanthose of stool samples in determining faecal carriage [15]The swabs were then cultured on specific chromogenic agarmedia (ChromID ESBL Biomerieux Marcy lrsquoEtoile France)ESBL detection was done according to CLSI guidelinesusing disk diffusion test for cefotaxime and ceftazidimealong with amoxicillin-clavulanic acid [19] for detection ofsynergy (keyhole effect) in a double disk synergy methodPossible Amp C resistance was detected by cefoxitin disksCiprofloxacin disks were used to test for quinolone resistanceThe identification of all the strains was done using API20E kit (Biomerieux France) Finally all isolated strains

were preserved in a ltndash80∘C freezer in cupules containing acombination of nutrient broth (85) and glycerol (15)

The medical records of all participants were checkedat the beginning of the study A questionnaire was usedto gather details about patientsrsquo age gender length of stay(LOS) at the nursing home diagnosis on admission mobilitystatus comorbidities (neurologic diseases diabetes cancercardiovascular diseases pulmonary diseases and under-lying urogenital pathologies) bladderbowel incontinenceindwelling medical devices (permanent and intermittenturinary catheters) and hospital admissions during the lastyear and antibiotic treatments in the preceding 3 monthsAt NH1 the faecal carriage was reexamined and the medicalrecords were reviewed every 6 weeks to note any alterationin the medical condition A case of ESBL faecal carriagewas defined as an individual who had at least one positivecarriage All NH1 participants were monitored for the onsetof any UTI to examine whether it was an infection with anESBL-producing strain A UTI is an infection involving anypart of the urinary system including urethra bladder uretersprostate and kidneys A case definition of a UTI consists ofclinical (dysuria urgency frequency suprapubic tendernessand flank pain) and microbiological (pure culture of a singlemicroorganism and a colony count higher than 105 colonyforming units per mL) findings

24 Statistics and Data Analysis Classical descriptive meth-ods were used for univariate analysis for the whole sampleand according to the study site Continuous variables (agelength of stay) were described using means medians andstandard deviations Categorical data were summarized usingproportions Additionally bivariate analysis was performedto compare different variables according to the carriagestatus Quantitative data were compared using Studentrsquos 119905-testor Mann-Whitney 119880 test when appropriate Qualitative datawere compared using Chi-square or Fisherrsquos exact test whenappropriate Analysis was performed for each site alone 119875values below 005 were considered statistically significant Noadjustment formultiple comparisonswasmade All statisticalcalculations were performed using SPSS V20 (IBM SPSSStatistics 200)

3 Results

31 Prevalence and Dynamics of ESBL Faecal Carriage Theoverall number of individuals included in the study at leastonce during the 3 phases at NH1 was 57 At NH2 a one-timerectal swabbing took place in August 2012 and 151 residents(755 of eligible individuals) signed the consent form Theparticipantsrsquo demographic and medical data are presented inTable 1 In NH1 at 119879

0 26 of 52 residents (50) were positive

for ESBL faecal carriage At 1198791 32 of 53 residents (604)

were positive Finally at 1198792 38 of 51 residents (745) were

positive Overall 46 of 57 individuals (807) were at leastone-time carriers during the follow-up time while only 11 of57 individuals (193)were never carriers Between119879

0and1198791

the ESBL faecal carriage disappeared in 5 residents (102)while 9 residents (184) acquired this carriage Between 119879

1




Male 19 (333) 54 (358)Female 38 (667) 97 (642)














506040

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0

10

20

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50

60

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80

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Prevalence ()


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daggerb50 (117)

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Male 19 (333) 54 (358)Female 38 (667) 97 (642)














506040

74506821 716

0

10

20

30

40

50

60

70

80

()


Prevalence ()


1020

6

1840 20

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500

1000

1500

2000

2500

()











daggerb50 (117)

daggerb







daggerc3 (63)

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119875 =


4 Discussion










252930

1280

2260

0

5

10

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20

25

30

35

()






References











































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OncologyJournal of





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Journal of

ObesityJournal of





















daggerb50 (117)

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119875 =


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1280

2260

0

5

10

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20

25

30

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OncologyJournal of





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ObesityJournal of





















252930

1280

2260

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OncologyJournal of





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OncologyJournal of





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OncologyJournal of





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Journal of

ObesityJournal of





















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OncologyJournal of





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Journal of

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