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Management of the Catheter in Documented Catheter-Related Coagulase-Negative Staphylococcal Bacteremia: Remove or Retain?

  1. Issam Raad1,
  2. Rawan Kassar1,
  3. Dany Ghannam2,
  4. Anne Marie Chaftari1,
  5. Ray Hachem1, and
  6. Ying Jiang1
  1. 1The University of Texas M. D. Anderson Cancer Center, Houston
  2. 2Kadlec Medical Center, Richland, Washington
  1. Reprints or correspondence: Dr Issam Raad, 1515 Holcombe Blvd, Unit 1460, Houston, TX 77030 (iraad{at}mdanderson.org).
 
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Abstract

Background. Studies and guidelines recommending the retention of the central venous catheter (CVC) in patients with coagulase-negative staphylococcal bacteremia were based on loose definitions of bacteremia and/or did not evaluate the risk of recurrence. In this study, we used strict definitions of coagulase-negative staphylococcal bacteremia to determine the impact of CVC retention on response to and recurrence of infection.

Methods. During the period from July 2005 through December 2007, we retrospectively evaluated 188 patients with coagulase-negative staphylococcal bacteremia. Bacteremia was defined using the strict Centers for Disease Control and Prevention criteria of 2 positive blood culture results. Catheter-related bacteremia was confirmed by differential quantitative blood cultures (⩾3:1) or time to positivity (>2 h).

Results. Resolution of infection within 48 h after commencement of antimicrobial therapy was not influenced by CVC removal or exchange versus retention and occurred in 175 patients (93%). Multiple logistic regression analysis showed that infection was 7.0 times (95% confidence interval [CI], 1.5–32.6 times) more likely to fail to resolve in patients with an intensive care unit stay prior to infection (P=.013) and 3.8 times (95% CI, 1.1–13.3 times) more likely to fail to resolve in patients who had other concurrent sites of infection (P=.041). Duration of therapy did not affect recurrence. Multiple logistic regression analysis revealed that patients with catheter retention were 6.6 times (95% CI, 1.8–23.9 times) more likely to have a recurrence than were those whose catheter was removed or exchanged (P=.004).

Conclusions. CVC retention does not have an impact on the resolution of coagulase-negative staphylococcal bacteremia but is a significant risk factor of recurrence.

Coagulase-negative staphylococci (CoNS) were long thought to be clinically unimportant organisms of low virulence, particularly because they are commensal skin organisms that often contaminate clinical microbiology laboratory specimens, such as blood culture samples [1–3]. These organisms are now considered the most commonly reported pathogens to cause nosocomial bloodstream infection in hospitalized patients [4, 5].

In addition, biofilm-forming CoNS are the leading cause of central venous catheter (CVC)-related bloodstream infection (CRBSI) [6–10]. CoNS adhere to the surface of the catheter through the formation of a multilayered biofilm matrix in which they embed themselves [6–8]. Once the biofilm layer is formed, eradication of catheter colonization without removal of the catheter is difficult, because the microbial cells embedded in the biofilm matrix are protected from the antimicrobial activity of various antibiotics, including vancomycin [11–16].

Current guidelines by the Infectious Diseases Society of America (IDSA) on the management of intravascular catheters in patients with CRBSI do not recommend routine removal of the CVC [17]. However, the recommendations are based on studies that used a less-than-strict definition of CoNS CRBSI and focused only on the acute resolution of the infection rather than on the risk of recurrence [18, 19].

To determine the impact of CVC removal on the management of CoNS CRBSI, we studied 188 patients with documented CoNS CRBSI based on strict definitions, and we assessed outcome in terms of resolution and recurrence of the infection.

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Methods

Clinical characteristics. We conducted a retrospective chart review of patients with CoNS CRBSI treated at The University of Texas M. D. Anderson Cancer Center (Houston) during the period from July 2005 through December 2007. Patients were identified through a search of the microbiology laboratory database. Patients with polymicrobial bloodstream infection or other concomitant infection at the time of presentation were excluded from the study. With use of an electronic chart review and the infection control database, clinical and microbiology laboratory data were obtained during the inpatient stays and follow-up visits, up to 4 months after the initial case of bacteremia, as outlined in Tables 1–3.

Figure 1
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Figure 1

Estimated cumulative incidence curves with coagulase-negative staphylococcal bacteremia recurrence (A; P<.001) and death (B; P=.73) based on competing risk analysis of recurrence and death for patients whose catheters were retained and those whose catheters were removed or exchanged after onset of bacteremia. CVC, central venous catheter.

Table 1
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Table 1

Univariate Analysis of Patients with Coagulase-Negative Staphylococcal Bacteremia Who Had Complications versus Those Who Did Not Have Complications

Information regarding the catheter was obtained using Netpass (Jolly Giant Software) and electronic medical charts. Netpass is an application used at our institution for accessing the patient care system that allows the user to access all patients' catheter information. The type, site, time of insertion of the catheter, management of the catheter at the time of bacteremia, and number of days to defervescence according to catheter removal or exchange were recorded. Microbiology laboratory data included: time to positivity of cultures and the number of colony-forming units (CFU) for both the CVC and the peripheral vein.

Lysis centrifugation quantitative blood culturing was performed using the Isolator 10 system (Wampole Laboratories). Each blood culture set consisted of 10 mL of whole blood collected into the Isolator 10 tube and 10 mL added to a Bactec 26 Plus resin bottle (Becton Dickinson). The isolator tubes were brought to the laboratory within 4 h and processed according to the manufacturers recommendations. Colony growth was evaluated using Gram stain, the Staphaurex test (Murex Diagnostics), L-pyrolidonyl-p-naphthylamide hydrolysis, optochine susceptibility test, oxidase test, and motility test, as necessary; colonies were identified using the Vitek AMS Instrument (bioMérieux)

Blood culture bottles were taken promptly to the microbiology laboratory and placed in an automatic culture detector (Bactec 9240 and Bactec Plus Aerobic/F; Becton Dickinson), which records culture positivity every 15 min according to changes in fluorescence related to microbial growth.

Study definitions. In addition to the clinical signs and symptoms of infection (fever, chills, rigors, or hypotension), true CoNS CRBSI was defined on the basis of the following 3 criteria, which are predictive of true bacteremia: (1) at least 2 blood cultures, from any source, should be available for all patients [2, 20–22]; (2) at least 1 blood culture should yield a quantitative blood count of ⩾15 CFU/mL [23]; and (3) the blood samples that yielded positive culture results should have been collected within a 72-h period [24]. Bacteremia also had to fulfill the definition criteria of the IDSA for probable or definite CRBSI [17].

Resolution was defined as cessation of all clinical signs and symptoms associated with bacteremia, together with microbiological eradication of CoNS from the bloodstream within 48 h after the initiation of adequate therapy. Adequate therapy was defined as initiation of systemic antibiotics that are active against the organism isolated on the basis of the hospital susceptibility pattern.

Recurrence was defined as the occurrence of at least 1 episode of CoNS bacteremia after resolution of the initial case of bacteremia and within 1 week to 4 months after the date of the initial bacteremia or until death, if it occurred during the 4-month follow-up period. The CoNS had to have an antibiogram similar to the initial isolate associated with clinical signs and symptoms, whereas relapse was defined as the recurrence of bacteremia with the same strain, as defined by pulse-field gel electrophoresis.

Attributable mortality was defined as bacteremia-related death, with microbiological evidence of infection at the time of death or evidence of infection at autopsy.

Statistical analysis. The χ2test or the Fisher exact test was used to compare categorical variables, as appropriate. Continuous variables were compared using the Wilcoxon rank sum test because of the deviation of the data from normal distribution. In addition, multiple logistic regression method was used to identify the factors associated with infection resolution and recurrence. All potential prognostic factors described above were evaluated for infection resolution. First, univariable analyses were performed to evaluate the predictive effect of each factor alone. Then, any factor for which the univariable test yielded a P value <.25 was included in a full multiple logistic regression model. Finally, the full model was reduced by a backward selection procedure at a significance level of 5%. Furthermore, competing risk analysis was performed for the patients whose infection resolved. Patients were observed for 4 months from the onset of CoNS bacteremia, and the competing events were CoNS bacteremia recurrence and death. The cumulative incidence curves for patients whose catheters were retained and those whose catheters were removed or exchanged were estimated, and their equality was compared. All tests were 2-sided, and statistical significance was defined as a P value ⩽.05. The competing risk analysis was performed using the statistical software R, version 2.8.1 ( http://cran.cnr.Berkeley.edu) [25], and all other statistical analyses were performed using SAS software, version 9.1 (SAS Institute).

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Results

Patients and complications. We evaluated 910 positive blood cultures for CoNS. Forty-one cultures were excluded because the patient had polymicrobial or concomitant infection at the time of presentation. One hundred eighty-eight patients with documented CRBSI met the clinical and microbiological criteria to be eligible for the study. Of the 188 patients, 141 (75%) had blood obtained from both the CVC and peripheral vein, 25 (13%) had blood obtained from the CVC only, and 22 (12%) had blood obtained from the peripheral vein only.

The clinical characteristics of patients with CRBSI are described in Table 1. Five patients had a complicated course of CRBSI: 4 patients had evidence of septic phlebitis of the great vein, and 1 patient had endocarditis. No other significant differences were noted.

CoNS isolates were available for 81 patients; speciation revealed a predominance of Staphylococcus epidermidis (93%), followed by Staphylococcus hominis (5%), Staphylococcus capitis (1%), and Staphylococcus caprae (1%). There were no differences between patients who had complications versus those who did not have complications in terms of causative agents.

Resolution and immediate outcome. Of the 188 patients with bacteremia, bacteremia resolved in 175 and did not resolve in 13 (Table 2). Twenty-seven deaths (16%) occurred ⩽4 months after onset of bacteremia in patients whose bacteremia resolved, compared with 10 deaths (77%) among those whose bacteremia did not resolve (P<.001). However, of the deaths with known causes, only 1 death was partially attributed to the CoNS bacteremia. More patients (62%) in the nonresolution group had other sites of infection, compared with patients in the resolution group (41%) (P=.08). There were no differences between the 2 groups in terms of underlying species. However, the duration of neutropenia and the likelihood of being in the intensive care unit (ICU) were significantly greater for patients whose bacteremia did not resolve than for those whose bacteremia did resolve (P<.05) (Table 2).

Table 2
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Table 2

Univariate Analysis of Patients with Central Venous Catheter-Associated Coagulase-Negative Staphylococcal Bloodstream Infection Whose Infection Resolved versus Those Whose Infection Did Not Resolve

Regarding outcomes, patients without resolution were more likely to enter the ICU during the infection than were those with resolution (62% vs 8%; P<.001).

Multiple logistic regression analysis revealed that patients with an ICU stay prior to infection were 7 times (95% confidence interval [CI], 1.5–32.6 times) more likely to not achieve resolution (P=.013), compared with patients without ICU experience. Patients who had other current sites of infection were 3.8 times (95% CI, 1.1–13.3 times) more likely to not achieve resolution (P=.041) than were those without other current sites of infection. In addition, management of the catheter (retention vs removal or exchange) did not have a significant impact on the immediate resolution of the infections (Table 2).

Recurrence and long-term outcome. The 175 patients who achieved resolution were observed for recurrence for up to 4 months after the initial episode of bacteremia. Of those, 17 patients had recurrence, 136 did not, and the other 22 were lost to follow-up for various reasons (eg, the patients entered hospice care or moved out of state). The cumulative duration of follow-up for the entire cohort was 17,035 days, with a median of 122 days (range, 3–122 days). Among those patients with recurrence, isolates were analyzed for only 6 patients and were all identical to the CoNS strains that caused the original case of bacteremia. Of the 17 patients with recurrence, 12 (71%) were hospitalized for a median duration of 10 days (range, 3–35 days), 16 patients (94%) received antibiotic therapy for their recurrence episode for a median duration of 8 days (range, 1–19 days), 3 patients (18%) developed thrombophlebitis, and 1 patient (6%) had an infection-related death.

On the basis of the univariate analyses, the recurrence and the nonrecurrence groups had comparable demographic characteristics, clinical characteristics, and underlying species. However, patients who experienced recurrence were younger than those who did not (median age, 38 vs 56 years; P=.004). Patients who experienced recurrence more frequently had CVCs retained (76% vs 35%; P=.001) and were more likely to have infusion ports (35% vs 7%; P=.002) (Table 3). The rate of use of tunneled catheters was similar in the 2 groups (6% vs 6%; P>.99).

Table 3
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Table 3

Univariate Analysis of Patients with Bacteremia Recurrence ⩽4 Months after Onset versus Those with Nonrecurrence

Multiple logistic regression analysis revealed that 3 factors were independently associated with recurrence: cancer type, catheter management, and catheter type. However, patients with hematologic cancer and those with solid tumors did not have statistically significant differences in the rate of recurrence (P=.21). Patients whose catheters were retained were 6.6 times (95% CI, 1.8–23.9 times) more likely to experience recurrence, compared with patients whose catheters were removed or exchanged (P=.004). In addition, the competing risk analysis showed that the cumulative incidence curves for recurrence were significantly different between the catheter retention group and the catheter removal or exchange group (P<.001) (Figure 1A). Patients whose catheters were retained had a higher probability of recurrence ⩽4 months after infection. Patients with a Port-a-Cath were 15.1 times (95% CI, 3.2–70.2 times) more likely to experience recurrence than were those with nontunneled catheters in place (P=.006). Multiple logistic regression analysis also demonstrated that age—although it was found to be significantly associated with recurrence in univariate analysis—was not independently associated with recurrence after adjustment for other factors, such as catheter management and catheter type.

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Discussion

In this study that included 188 patients with true CoNS CRBSI, with 2 blood cultures positive for CoNS, as well as high quantitative blood cultures for this organism (>15 CFU/mL), it was determined that the CVC retention did not have an impact on the acute resolution of the infection but is an independent risk factor for the recurrence of bacteremia. Another independent factor that was significantly associated with recurrence of bacteremia by multiple logistic regression analysis was the use of ports. Factors that were associated with failure to achieve acute resolution and response to antimicrobial therapy were critically ill status and other concurrent sites of infection.

It is well established that CoNS organisms adhere to the catheter surface through the production of a microbial biofilm [6–8, 10]. Embedded in this microbial biofilm matrix, the CoNS are difficult to eradicate through the use of active agents that are often used in the treatment of CoNS bacteremia, such as glycopeptides (including vancomycin) [9, 11–16]. Given the pathogenesis of CoNS CRBSI based on biofilm and the role of biofilm acting as a resistance factor, it is not surprising that the colonized indwelling CVC that is acting as the source of the CRBSI will act as the source of recurrence of CoNS bacteremia unless it is removed or exchanged.

Most of the studies that concluded that CoNS bacteremia may be treated without catheter removal had several limitations. First, many of these studies did not include a strict definition of true, documented CoNS bacteremia and CRBSI and, in some instances, included possible blood culture contamination [18, 19]. Febrile high-risk patients, such as the critically ill patients or patients with cancer, may often have blood cultures contaminated with CoNS from the hands of medical personnel or the catheter hub, particularly if the blood specimens are drawn from the CVC [26, 27]. Use of strict criteria for the definition of CoNS bacteremia that include 2 blood cultures positive for CoNS as well as high quantitative blood cultures (>15 CFU/mL) has been shown to be important for distinguishing true CoNS bacteremia from contaminated blood cultures [2, 20–23]. Furthermore, use of strict criteria for CRBSI, as per the IDSA guidelines, is necessary to attribute true CoNS bacteremia to the catheter rather than other sources that could exist in patients with cancer who have long-term catheters in place [17].

All of the 188 patients included in this current study had 2 specimens that yielded positive blood culture results drawn within a time period of 72 h, with at least 1 quantitative blood culture yielding >15 CFU/mL. In addition, a study conducted at our center showed a strong concordance of phenotypic and genotypic CoNS organisms isolated from positive blood culture results of specimens drawn within a 72-h period from the same patient; thus, such a criterion was used in this current study as confirmation of true CoNS bacteremia [24]. In another study conducted at our center, we demonstrated that positive blood culture results with >15 CFU/mL of CoNS are highly suggestive of true CoNS bacteremia [23]. We have also adopted the IDSA definitions of CRBSI that included evidence-based criteria that strongly suggest that the CoNS bacteremia is catheter related as a requirement for all patients included in this study [17].

Another limitation of previous studies or guidelines that concluded that CVCs may be retained in patients with CoNS CRBSI is that they focused on the evaluation of acute resolution of the infection as the only end point [18, 19, 28]. There are several possible explanations as to why CVC retention did not worsen the outcome in terms of the acute resolution of CoNS CRBSI. First, CoNS, unlike Staphylococcus aureus , are less likely to invade tissues or result in deep-seated infections, such as endocarditis [28, 29]. Second, the commonly used antibiotics for treatment of CoNS bacteremia (eg, vancomycin) are quite active against free-floating CoNS organism in the bloodstream; this determines the immediate outcome as far as acute resolution of the infection. However, given the fact that many of antibiotics used for treatment of CoNS CRBSI—particularly vancomycin—fail to completely eradicate the CoNS organism embedded in biofilm on the surface of the indwelling catheter, one can appreciate why CVC retention in patients with CoNS CRBSI is associated with a higher rate of recurrence [9, 11–16]. In support of our data, several other studies have demonstrated that CVC retention in CoNS CRBSI does not affect the associated acute mortality or acute resolution of the infection; however, CVC retention was significantly associated with a higher rate of recurrence of bacteremia [30–32].

The IDSA guidelines on the management of intravascular CoNS CRBSI teach that, if the culprit indwelling CVC is retained, then systemic antibiotic therapy should be extended to a duration of at least 10 days [17]. However, data from our study show that a more prolonged treatment, including a treatment duration of >10 days, was not associated with better resolution of acute bacteremia or a significantly lower rate of recurrence. This finding is in contrast to the study by Flynn et al [32], who reported a trend toward a lower recurrence rate associated with >10 days of systemic antibiotic therapy (P=.07).

However, another observation in the current study, which is similar to that observed by Flynn et al [32], is that infusion ports causing CoNS CRBSI were more frequently associated with recurrence of the infection. We, therefore, agree with Flynn and colleagues' conclusion that “intimate contact between the needle puncture of the port and the superficial skin is a direct pathway for the organism to gain entry into the port” (p. 3524). Organisms in the lumen of the port valve/bell will form a solid biofilm that will be quite difficult to clear with systemic intravenous antibiotics alone without of removal of the port.

This study is subject to several limitations. The first is its retrospective, nonrandomized design. Patients were not on a defined clinical protocol requiring routine blood cultures during the infection and thereafter; this can lead to underestimations of the duration of true infection and recurrence. Another limitation is lack of availability of all of the CoNS organisms associated with recurrence for genotypic DNA typing. Only 6 of the 17 patients who experienced recurrence had their isolates typed and were considered to have experienced relapsed, because the isolates were identical to the original CoNS isolate causing the initial bacteremia. Thus, we have used the term recurrence in this study instead of relapse .

In conclusion, although CVC retention does not have an impact on the acute resolution of CoNS CRBSI, it is associated with a significantly higher rate of recurrence. In patients with a limited vascular access or those with hypocoagulable state (such as thrombocytopenia) for whom removal of the CVC is not possible, additional investigations through well-designed studies should determine the efficacy and safety of salvage interventions. Among the salvage interventions to be studied will be the exchange of the culprit CVC over guidewire for a new antimicrobial catheter (in patients with an exchangeable catheter) or use of effective antimicrobial lock therapy in patients with nonexchangeable, surgical, implantable catheters, such as ports.

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Acknowledgments

Potential conflicts of interest. I.R. has received grants from Cubist, Pfizer, and Wyeth; has served as a consultant to Cubist; and has served on the speakers' bureau for Pfizer and Cook Industries (speakers' bureau service, consultancies, grants, and royalties related to patents licensed to Cook on which I.R. is an inventor or coinventor). All other authors: no conflicts.

  • Received October 7, 2008.
  • Accepted June 6, 2009.
  • Final version accepted September 22, 2009.
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  1. Clin Infect Dis. (2009) 49 (8): 1187-94. doi: 10.1086/605694
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