This prospective randomized controlled study with 975 nontunneled central venous catheters (CVCs) showed that the semiquantitative roll-plate culture technique (SQC) was as accurate as the sonication method for diagnosis of catheter-related infections. Sonication is difficult to standardize, whereas SQC is simpler, faster, and as reliable as the sonication method for culturing CVC

Dangel, Marc

Erb, Stefan

Frei, Reno

Nogarth, Danica

Schregenberger, Katharina

Widmer, Andreas F.

RERO DOC Digital Library

B R I E F R E P O R TSonication for Diagnosis ofCatheter-Related Infection Is NotBetter Than Traditional Roll-PlateCulture: A Prospective Cohort StudyWith 975 Central Venous CathetersStefan Erb,1 Reno Frei,2 Katharina Schregenberger,1 Marc Dangel,1Danica Nogarth,1 and Andreas F. Widmer1Divisions of 1Infectious Diseases and Hospital Epidemiology and 2ClinicalMicrobiology, University Hospital Basel, SwitzerlandThis prospective randomized controlled study with 975 non-tunneled central venous catheters (CVCs) showed that thesemiquantitative roll-plate culture technique (SQC) was asaccurate as the sonication method for diagnosis of catheter-related infections. Sonication is difﬁcult to standardize,whereas SQC is simpler, faster, and as reliable as the sonica-tion method for culturing CVCs.Keywords. semiquantitative roll-plate method; sonication;central venous catheter; catheter-related bloodstream infections.The diagnosis of catheter-related infection requires a positiveresult by the semiquantiative roll-plate culture method (SQC)described by Maki et al [1] or the quantitative sonication tech-nique [2, 3] of the central venous catheter (CVC) and a match-ing strain from percutaneously drawn blood cultures in cases ofcatheter-related bloodstream infection (CR-BSI). Both tech-niques are recommended in the current Centers for DiseaseControl and Prevention and Infectious Diseases Society ofAmerica guidelines for diagnosis and management of catheter-related infections as equivalent methods [4, 5]. Sonication isconsidered to have a higher sensitivity than SQC by detectingintraluminal and extraluminal bacteria, whereas SQC only de-tects extraluminal bacteria [6–8]. However, more recent studieswere unable to conﬁrm the advantage of the sonication method,even in tunneled long-term catheters where endoluminal con-tamination is thought to be the most frequent route of microbialcolonization [9–11]. Furthermore, sonication is time-consuming,difﬁcult to standardize, and complicated to perform.In a prospective, observational, randomized controlled trialfrom 2005 until 2009 at the University Hospital of Basel,Switzerland, we compared the SQC with the quantitative soni-cation method for diagnosis of signiﬁcant catheter colonization.MATERIALS AND METHODSAll consecutive nontunneled CVCs with aminimal length of 10 cmwere included in our study. CVCs were cut into 2 equal 5-cm-sized segments, in a subcutaneous part and a catheter tip, andrandomly processed with the SQC by Maki et al [1] and animproved quantitative sonication method published elsewhere[12]. Randomization occurred in the microbiology laboratory:On even days, the catheter tip was processed by the roll plateand the subcutaneous segment of the catheter was processedwith the sonication method, and vice versa on odd days.Catheter colonization was deﬁned as ≥15 colony-formingunits (CFU) per 5-cm-sized catheter segment for the SQCand/or ≥100 CFU per 5-cm-sized catheter segment for sonica-tion [1, 4, 6]. Our data were also recalculated using different cut-offs of ≥5 CFU for SQC and ≥1000 CFU for sonication.Diagnosis of CR-BSI was based on current guidelines [4, 13]and required a catheter tip colonization as described above, withthe same phenotypic microorganism isolated from blood cul-ture or a differential time to positivity of ≥2 hours for the pe-ripheral vs the CVC blood culture. For CR-BSI with skincontaminants such as coagulase-negative staphylococci, system-ic inﬂammatory response syndrome (SIRS) with at least 2 SIRScriteria had to be present [14].We calculated a sample size of >800 CVCs to detect an abso-lute 5% difference with 90% power. Paired proportions fromcatheters were compared using the McNemar test with 95%conﬁdence intervals (CIs). Continous variables from indepen-dent patient data were analzed by Student t test. A P value of<.05 was considered to be statistically signiﬁcant. Data were an-alyzed using the SPSS software package, version 21.0.RESULTSA total of 975 nontunneled CVCs from 800 patients were exam-ined with both the SQC and the new sonication method. TheReceived 9 January 2014; accepted 3 May 2014; electronically published 13 May 2014.Correspondence: Andreas F. Widmer, MD, MS, Division of Infectious Diseases and HospitalEpidemiology, University Hospital Basel, Petersgraben 4, 4031 Basel, Switzerland (andreas.widmer@usb.ch).Clinical Infectious Diseases 2014;59(4):541–4© The Author 2014. Published by Oxford University Press on behalf of the Infectious DiseasesSociety of America. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.DOI: 10.1093/cid/ciu352BRIEF REPORT • CID 2014:59 (15 August) • 541SQC was performed in 481 (49.3%) catheter tips and 494(50.7%) subcutaneous segments, and vice versa with the sonica-tion method.Signiﬁcant colonization was detected in 217 of the 975 (22.3%)catheters with at least 1 of the 2 methods by use of currentlyrecommended cutoff of ≥15 CFU for SQC and ≥100 CFU forsonication. Fifty-two (24%) patients had a CR-BSI that fulﬁlledstudy criteria. The remaining 165 catheters were derived from pa-tients with secondary bloodstream infections not related to thecatheter or asymptomatic patients without signs of infection(for baseline characteristics, see the Supplementary Table).When using the established cutoff of ≥15 CFU for SQC and≥100 CFU for the sonication method, the SQC method detect-ed colonization in 190 (87.6%) and sonication detected coloni-zation in 184 (84.8%) of the 217 catheters (Table 1). Discrepantresults occurred in 27 (SQC positive, sonication negative) and in33 (SQC negative, sonication positive) processed catheters.Thus, no signiﬁcant difference of likelihood of detection be-tween the 2 methods could be found (odds ratio [OR], 0.82[95% CI, .49–1.36]; P = .52).When using a lower cutoff of ≥5 CFU for the SQC method,the detection rate of SQC increased to 91.9%, which wasTable 1. Detection Rate of Catheter Colonization in All 975 Examined Catheters by Use of Different Cutoffs Between SemiquantitativeCulture and SonicationSQC ≥15 CFU and/or Sonication ≥100 CFU (n = 217) SQC ≥5 CFU and/or Sonication ≥100 CFU (n = 235)SQC+ SQC− SQC+ SQC−Sonication+ 157 27 184 Sonication+ 165 19 184Sonication− 33 758 791 Sonication− 51 740 791190 785 975 216 759 975OR, 0.82 (95% CI, .49–1.36); P= .52 OR, 0.37 (95% CI, .22–.63); P< .001SQC ≥5 CFU and/or Sonication ≥1000 CFU (n = 224) SQC ≥15 CFU and/or Sonication ≥1000 CFU (n = 203)SQC+ SQC− SQC+ SQC−Sonication+ 122 8 130 Sonication+ 118 12 130Sonication− 94 751 845 Sonication− 73 772 845216 759 975 191 784 975OR, 0.085 (95% CI, .04–.18); P< .001 OR, 0.16 (95% CI, .09–.30); P< .001Abbreviations: CFU, colony-forming units; CI, confidence interval; OR, odds ratio; SQC, semiquantiative culture.Table 2. Detection Rate of Catheter Colonization by Semiquantitative Culture and SonicationaCVCs With a Dwelling Time >7 d (n = 165) CVCs With a Dwelling Time ≤7 d (n = 52)SQC+ SQC− SQC+ SQC−Sonication+ 119 19 138 Sonication+ 38 8 46Sonication− 27 0 27 Sonication− 6 0 6146 19 165 44 8 52OR, 0.70 (95% CI, .39–1.27); P= .30 OR, 1.33 (95% CI, .46–3.84); P= .79CVCs From Patients With CR-BSI (n = 52)SQC+ SQC−Sonication+ 37 7 44Sonication− 8 0 845 7 52OR, 0.875 (95% CI, .32–2.41); P= 1.00Abbreviations: CI, confidence interval; CR-BSI, catheter-related bloodstream infection; CVCs, central venous catheters; OR, odds ratio; SQC, semiquantiative culture.a SQC cutoff of ≥15 colony-forming units (CFU) and sonication cutoff ≥100 CFU in the subgroup of patients with CVC dwelling time >7 and ≤7 days and patientswith CR-BSI.542 • CID 2014:59 (15 August) • BRIEF REPORTsigniﬁcantly better compared with sonication with a cutoff of≥100 CFU and ≥1000 CFU (both P < .001). By raising the son-ication cutoff to ≥1000 CFU (with cutoff ≥15 CFU for SQC),the performance of this method became worse compared withSQC (P < .001; Table 1).From the 217 CVCs with signiﬁcant colonization using a cut-off of ≥15 CFU for SQC and/or ≥100 CFU for sonication, 52(24.0%) were in place for a short time (≤7 days), and 165(76.0%) were in place for >7 days (Table 2). In both of thesegroups, SQC showed noninferiority to sonication (P = .79 andP = .30, respectively).In the 52 patients with CR-BSI, 45 (86.5%) and 44 (84.6%)CVCs were found to be colonized by the SQC and the sonica-tion technique, respectively; thus, the likelihood of detection didnot differ between the 2 methods (P = 1.00; Table 2).The likelihood of detection of colonization between SQC andthe sonication method was similar in subclavicular (OR, 1.50[95% CI, .534–4.24]; P = .607) and jugular (OR, 0.69 [95% CI,.38–1.263]; P = .291) CVCs, and also when examining the cathetertips (OR, 1.0 [95% CI, .46–2.18]; P = .85) and the subcutaneoussegments (OR, 0.70 [95% CI, .35–1.39]; P = .35) (data not shown).The distribution of the 217 isolated main pathogens showed apredominance of coagulase-negative staphylococci, followed bygram-negative bacteria and Staphyloccoccus aureus (Table 3).When comparing the 2 methods, coagulase-negative staphylococciwere more frequently detected by SQC (OR, 0.5 [95% CI, .26–.95];P = .045), whereas gram-negative bacteria were better detected withthe sonication method (OR, 9.0 [95% CI, 1.14–71.04]; P = .021).DISCUSSIONIn this randomized controlled study of 975 nontunneled CVCs,we demonstrated that the use of an improved quantitative sonica-tion technique [12] to detect catheter colonization is not superiorto the SQC method by Maki et al when using a recommendedcutoff of ≥15 CFU for SQC and ≥100 CFU for sonication—neither in patients with a CR-BSI nor in catheters with a longdwelling time of >7 days. The noninferiority of the SQC methodas shown in our results is in accordance with the ﬁndings of otherrecent studies [9–11]. Furthermore, the quantitative sonicationmethod requires special equipment, is difﬁcult to standardize,and is time-consuming and complicated to perform, making itless attractive for routine microbiological catheter diagnostics.The strength of our study is the large sample size of almost1000 CVCs that we could examine simultaneously with bothmethods at the same time on a 5-cm-sized catheter tip and ad-jacent subcutaneous segment. Hence, direct comparison of the2 methods is very reliable, whereas serial processing of cathetersby different detection methods as described in a former studysuffers from possible loss of microbial colonies during serial ex-amination [11].As the yield of detection of colonization of cath-eter tips and subcutaneous segments was similar as shown inTable 3. Frequency of Isolated Pathogens in All 217 Colonized CathetersaMicroorganismsTotal(n = 217)bSQC+/SONIC+(n = 157)SQC+/SONIC−(n = 33)SQC−/SONIC+(n = 27) P ValueCoNS 148 (68.2%) 106 28 14 .045*Staphylococcus aureusc 13 (6.0%) 12 1 0Enterococcus spp 7 (3.2%) 5 1 1Gram-positive bacteriad 4 (1.8%) 1 2 1Gram-negative bacteria 36 (16.6%) 26 1 9 .021**Enterobacteriaceae 26 18 1 7Pseudomonas aeruginosa 6 5 0 1Stenotrophomonas maltophilia 2 2 0 0Otherse 2 1 0 1Candida spp 9 (4.1%) 7 0 2SQC+: ≥15 colony-forming units (CFU); SQC−: <15 CFU; SONIC+: ≥100 CFU; SONIC−: <100 CFU.Abbreviations: CoNS, coagulase-negative staphylococci; SONIC, sonication; SQC, semiquantitative culture.aWith cutoffs of ≥15 CFU for SQC and ≥100 CFU for SONIC.b Main pathogen detected by at least 1 of the 2 methods of all 217 colonized catheters with cutoff of ≥15 CFU for SQC and ≥100 CFU for SONIC. Thirty-threecatheters had polymicrobial colonization with an additional 40 microorganisms detected with at least 1 of the 2 methods, but in a lesser amount than the mainpathogen: 26 CoNS, 7 Corynebacterium spp, 3 Streptococcus spp, 2 Enterococcus spp, 1 Stenotrophomonas maltophilia, and 1 yeast (not included in the table).c One S. aureus was methicillin-resistant.d Gram-positive bacteria: Streptococcus spp, Corynebacteria spp.e Gram-negative bacteria, others: Acinetobacter baumannii, Hafnia alvia.* Odds ratio (OR), 0.5 (95% confidence interval [CI], .26–.95).** OR, 9.0 (95% CI, 1.14–71.04).BRIEF REPORT • CID 2014:59 (15 August) • 543previous studies and in our own data [6], the comparison ofcatheter tip and subcutaneous segment cultures is most likelyappropriate.When analyzing our results with different cutoffs for bothmethods, the SQC was always equal or better than sonicationin the detection of catheter colonization. However, the addition-al beneﬁt of a lower SQC cutoff of ≥5 CFU/catheter segmentremains debatable due to loss of speciﬁcity, but could be usefulin antibiotic-pretreated patients.The distribution of the 217 pathogens in our study was as ex-pected. In case of polymicrobial catheter colonization, we only an-alyzed the main pathogen with the highest CFU count. As only 33catheters showed polymicrobial colonization, we considered thisapproach to be feasible. Whereas coagulase-negative staphylococ-ci were detected signiﬁcantly better by SQC, gram-negative bacte-ria were better detected with the sonication method. This isparticularly interesting because gram-negative bacteria are usuallymore susceptible than gram-positive bacteria to the effect of ultra-sound and thus more difﬁcult to detect [15]. Explanations remainhypothetical andmay imply a more gentle sonication technique, aweaker adhesion to the surface due to less bioﬁlm formation, or apotentially mainly endoluminal origin of gram-negative bacteria.However, in the subset of the 52 patients with CR-BSI, no diffe-rence was seen between the 2 methods.Our study has some limitations. We did not distinguish be-tween antimicrobial-coated and -uncoated CVCs in our study,which could have inﬂuenced the results; however, only 8% ofthe analyzed CVCs were submitted from the transplant unit,where coated catheters are routinely inserted. In addition,only ﬁrst-generation chlorhexidine/silver sulfadiazine–coatedCVCs are used that are coated only at the outer surface of thecatheter. But this would have rather lowered the sensitivity ofthe SQC method.Furthermore, we did not collect data about administered sys-temic antibiotics over the CVC that could have inﬂuenced thecolonization rate. It is well known that antimicrobial treatmentcan lower the diagnostic yield of catheter tip culture. As the an-tibiotics are usually administered through the catheter, endolu-minal microbes might be compromised more than extraluminalbacteria, which could impair the sensitivity of the sonicationmore than the roll-plate method [10].In conclusion, this prospective randomized controlled studywith 975 nontunneled CVCs showed that the SQCwas as accurateas the sonication method for diagnosis of catheter-related infec-tions. Sonication is difﬁcult to standardize, whereas SQC is sim-pler, faster, and as reliable as the sonication for culturing CVCs.Supplementary DataSupplementary materials are available at Clinical Infectious Diseases online(http://cid.oxfordjournals.org). Supplementary materials consist of dataprovided by the author that are published to beneﬁt the reader. The postedmaterials are not copyedited. The contents of all supplementary data are thesole responsibility of the authors. Questions or messages regarding errorsshould be addressed to the author.NotesFinancial support. The study was supported by the University Hospitalas part of the continous quality improvement program.Potential conﬂicts of interest. All authors: No reported conﬂicts.All authors have submitted the ICMJE Form for Disclosure of PotentialConﬂicts of Interest. Conﬂicts that the editors consider relevant to the con-tent of the manuscript have been disclosed.References1. Maki DG, Weise CE, Saraﬁn HW. A semiquantitative culture methodfor identifying intravenous-catheter-related infection. N Engl J Med1977; 296:1305–9.2. Sherertz RJ, Raad II, Belani A, et al. Three-year experience with sonicat-ed vascular catheter cultures in a clinical microbiology laboratory. J ClinMicrobiol 1990; 28:76–82.3. Cleri DJ, Corrado ML, Seligman SJ. Quantitative culture of intravenouscatheters and other intravascular inserts. J Infect Dis 1980; 141:781–6.4. Mermel LA, Allon M, Bouza E, et al. Clinical practice guidelines for thediagnosis and management of intravascular catheter-related infection:2009 update by the Infectious Diseases Society of America. Clin InfectDis 2009; 49:1–45.5. O’Grady NP, Alexander M, Burns LA, et al. Guidelines for the preven-tion of intravascular catheter-related infections. Am J Infect Control2011; 39(4 suppl 1): S1–34.6. Sherertz RJ, Heard SO, Raad II. Diagnosis of triple-lumen catheter in-fection: comparison of roll plate, sonication, and ﬂushing methodolo-gies. J Clin Microbiol 1997; 35:641–6.7. Raad II, Sabbagh MF, Rand KH, Sherertz RJ. Quantitative tip culturemethods and the diagnosis of central venous catheter-related infections.Diagn Microbiol Infect Dis 1992; 15:13–20.8. Siegman-Igra Y, Anglim AM, Shapiro DE, Adal KA, Strain BA, FarrBM. Diagnosis of vascular catheter-related bloodstream infection: ameta-analysis. J Clin Microbiol 1997; 35:928–36.9. Guembe M, Martín-Rabadán P, Echenagusia A, et al. How should long-term tunneled central venous catheters be managed in microbiologylaboratories in order to provide an accurate diagnosis of colonization?J Clin Microbiol 2012; 50:1003–7.10. Slobbe L, El Barzouhi A, Boersma E, Rijnders BJ. Comparison of the rollplate method to the sonication method to diagnose catheter coloniza-tion and bacteremia in patients with long-term tunnelled catheters: arandomized prospective study. J Cin Microbiol 2009; 47:885–8.11. Bouza E, Alvarado N, Alcala L, et al. A prospective, randomized, andcomparative study of 3 different methods for the diagnosis of intravas-cular catheter colonization. Clin Infect Dis 2005; 40:1096–100.12. Trampuz A, Piper KE, Jacobson MJ, et al. Sonication of removed hipand knee prostheses for diagnosis of infection. N Engl J Med 2007;357:654–63.13. Horan TC, Andrus M, DudeckMA. CDC/NHSN surveillance deﬁnitionof health care-associated infection and criteria for speciﬁc types of in-fections in the acute care setting. Am J Infect Control 2008; 36:309–32.14. Elzi L, Babouee B, Vogeli N, et al. How to discriminate contaminationfrom bloodstream infection due to coagulase-negative staphylococci: aprospective study with 654 patients. Clin Microbiol Infect 2012; 18:E355–61.15. Hua I, Thompson JE. Inactivation of Escherichia coli by sonication atdiscrete ultrasonic frequencies. Water Res 2000; 34:3888–93.544 • CID 2014:59 (15 August) • BRIEF REPORT

Sonication for Diagnosis of Catheter-Related Infection Is Not Better Than Traditional Roll-Plate Culture: A Prospective Cohort Study With 975 Central Venous Catheters

Sonication for Diagnosis of Catheter-Related Infection Is Not Better Than Traditional Roll-Plate Culture: A Prospective Cohort Study With 975 Central Venous Catheters

Abstract

Similar works

Full text

Available Versions

RERO DOC Digital Library