PEDIATRICS Vol. 121 No. 1 January 2008, pp. 135-141 (doi:10.1542/peds.2007-1387)
ARTICLE |
How Long Does It Take to "Rule Out" Bacteremia in Children With Central Venous Catheters?
Divisions of a Infectious Diseases and
d General Pediatrics and
h Clinical Microbiology Laboratory, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
Departments of b Epidemiology
c Pediatrics
j Medicine
i Pathology and Laboratory Medicine and
Centers for e Clinical Epidemiology and Biostatistics and
f Education and Research on Therapeutics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
k Veterans' Affairs Medical Center, Philadelphia, Pennsylvania
g Department of Biostatistics, University of Michigan School of Public Health, and Survey Methodology Program, University of Michigan Institute for Social Research, Ann Arbor, Michigan
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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BACKGROUND. Children with central venous catheters and suspected bloodstream infection are often hospitalized for 48 hours to receive empiric antibiotic therapy pending blood-culture results. Continuous monitoring blood-culture systems allow for more rapid detection of bloodstream infection than previous blood-culture systems, a feature that may facilitate earlier determination of the true presence or absence of bloodstream infection and shorten empiric antibiotic therapy and duration of hospitalization.
METHODS. This retrospective cohort study included children with central venous catheters who were diagnosed with laboratory-confirmed bloodstream infection after evaluation in the ambulatory care setting.
RESULTS. Two-hundred episodes of bloodstream infection were included. The median patient age was 5.5 years. Central venous catheters were in place for a median of 80.5 days. Gram-negative bacteria accounted for 51% of infections as part of either a monomicrobial (25%) or polymicrobial (26%) infection. The overall median time to blood-culture positivity was 14 hours. The predicted probability for a culture being positive at 36 hours was 99.2% for infections caused by Gram-negative bacteria and 96.6% for any infection after adjusting for age, catheter type, and recent antibiotic use. In a multivariate Cox proportional-hazards regression model, polymicrobial infections with 
1 Gram-negative bacteria and monomicrobial infections caused by Gram-negative bacteria were independently associated with an earlier time to blood-culture positivity after adjusting for age, catheter type, and recent antibiotic use.
CONCLUSIONS. The time to blood-culture positivity depends on bacterial category. Bloodstream infections caused by Gram-negative bacteria are detected most quickly. Our data suggest that discontinuation of empiric antibiotic coverage may be warranted in clinically stable children with central venous catheters if the blood-culture results remain negative 24 to 36 hours after collection.
Key Words: child • bacteremia • sepsis • central venous catheterization • blood culture
Abbreviations: CVC—central venous catheter • BSI—bloodstream infection • CMBCS—continuous-monitoring blood-culture system • HR—hazard ratio
Indications for central venous catheter (CVC) placement in children who are receiving therapy predominantly in the outpatient setting are diverse but commonly include administration of chemotherapy, blood products, parenteral nutrition, and antimicrobial agents. These children are at high risk of bloodstream infection (BSI) because of the presence of a CVC and underlying host factors.1 Children with CVCs and suspected BSI require immediate evaluation, because delay in initiation of appropriate antimicrobial therapy in patients with BSI can result in adverse outcomes, including death.2–4 As a consequence, these children are frequently hospitalized for 48 to 72 hours to receive empiric antibiotic therapy pending blood-culture results. Continuous-monitoring blood-culture systems (CMBCSs) permit more rapid detection of bacteria, a feature that may allow for an earlier determination of the true presence or absence of BSI and may shorten empiric antibiotic therapy and hospitalization.
Before the advent of automated CMBCSs, blood-culture bottles were manually examined once a day for macroscopic evidence of bacterial growth.5 Physicians waited >72 hours (3 readings) before discontinuing antibiotics or discharging patients admitted for evaluation of suspected BSI. In the 1980s, automated blood-culture instruments were introduced. These automated systems monitored the bottles twice each day and decreased the time to detect positive cultures. The clinical consequence of more frequent automated surveillance was that the duration of empiric antibiotic therapy could be shortened to 48 to 72 hours.6,7
Since 1990, several manufacturers have developed CMBCSs. These systems electronically monitor blood-culture bottles for evidence of microbial growth on a nearly continuous basis, typically once every 10 minutes.8 The availability of an automated CMBCS provides the opportunity to detect BSIs more rapidly than either noninstrument-based manual methods or automated systems not using continuous monitoring.9 Earlier detection or exclusion of BSIs can facilitate patient management decisions about the need for continued antibiotic therapy and, in some cases, duration of hospitalization.
Although CMBCSs allow for more rapid detection of BSIs, the results of current studies may not apply to children with CVCs. These studies have only been performed in otherwise healthy children.10–12 The time to bacterial detection may be more variable in children with CVCs who often have immunocompromising conditions. In addition, Streptococcus pneumoniae, the predominant pathogen in these previous studies, infrequently causes BSIs in children with CVCs, and the overall incidence of pneumococcal bacteremia in children has declined considerably since the introduction of the heptavalent conjugate vaccine.13,14 The time to pathogen detection may be more variable for organisms such as Staphylococcus species and enteric Gram-negative bacilli that commonly cause BSIs in children with CVCs. The objective of the current study was to describe the time to blood-culture positivity in children with CVCs evaluated for BSI in the ambulatory setting and to identify factors associated with the time to blood-culture positivity.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Study Design and Setting
This retrospective cohort study was conducted at the Children's Hospital of Philadelphia, an urban tertiary care children's hospital, between January 1, 2000, and December 31, 2003. The committees for the protection of human subjects approved this study with a waiver of informed consent.
Study Participants
Patients were eligible for inclusion if they were diagnosed with a laboratory-confirmed BSI after evaluation in the ambulatory care setting at the Children's Hospital of Philadelphia main campus. Ambulatory care sites included the emergency department, as well as all of the outpatient subspecialty clinics, including outpatient clinics of the hematology, oncology, gastroenterology, infectious diseases, and pulmonary medicine services. Patients with multiple admissions for BSI during the study period could be included more than once.
Dependent Variable
Time to blood-culture positivity was the primary dependent (outcome) variable.
Study Definitions
A patient was considered to have a laboratory-confirmed BSI if a recognized pathogen (eg, Staphylococcus aureus, enteric Gram-negative bacilli) was isolated from 1 blood culture or if the patient had signs or symptoms of systemic illness (fever >38°C, chills, or hypotension) and the same commensal bacterial species (ie, diphtheroids, Bacillus species, Propionibacterium species, coagulase-negative staphylococci, or micrococci) isolated from 2 blood cultures drawn on separate occasions. Bacteria were grouped into clinically relevant categories based on the presence or absence of Gram-negative bacteria and then further based on whether the infection was monomicrobial or polymicrobial. The time to blood-culture positivity was defined as the difference in hours between the time of blood-culture collection (as noted on the time-stamped laboratory specimen collection form) and the time that the blood culture was reported as positive by the BacT/Alert system (bioMérieux, Charbonnier les Bains, France). Because peripheral blood cultures are infrequently obtained from children with CVCs, only cultures obtained from the catheter were considered for the time-to-positivity calculation. For patients with multiple positive blood-culture results obtained during initial evaluation, the earliest positive culture was used for the time-to-positivity calculation. Receipt of antibiotics or parenteral nutrition was considered recent if it occurred within 72 hours of the time of blood-culture collection. A patient was considered to have had a recent BSI if a BSI was diagnosed within 30 days of evaluation for the current episode.
Study Protocol and Data Collection
The BacT/Alert system was used during the entire study period as a standard laboratory procedure. Blood was inoculated into pediatric blood-culture bottles (Pedi-BacT; Organon Teknika Corp, Durham, NC), which permit detection of aerobic and facultatively anaerobic bacteria, and subsequently transported to the Clinical Microbiology Laboratory and loaded into the blood-culture instrument. Carbon dioxide production was automatically monitored every 10 minutes, 24 hours per day.
Patients with a positive blood culture in the context of a CVC were identified by review of Clinical Microbiology Laboratory records; the source of the blood culture (peripheral versus CVC) is documented on all of the culture request forms and included in the laboratory records. The ambulatory medical chart and blood-culture results of all of the patients with positive blood-culture results obtained through a CVC were reviewed to identify those meeting the above-specified eligibility criteria. Study patients were randomly selected from all of the eligible patients. Each eligible patient was assigned a unique study number on the basis of the medical chart number and selected through the use of a computer-generated random-number table. The ambulatory and hospital medical charts of patients selected for study inclusion were reviewed for the following additional information: gender, age at BSI, comorbid medical conditions, catheter type, number of catheter lumens, date of catheter insertion, current receipt of immunosuppressive medications (eg, corticosteroids) or parenteral nutrition, receipt of antibiotics within 30 days before diagnosis, recent (within 7 days) health care visits, signs and symptoms at initial evaluation, results of initial laboratory evaluation, and blood-culture results.
Statistical Analysis
Data were analyzed by using Stata 9.2 (Stata Corp, College Station, TX). Categorical variables were described by using frequencies and percentages. Continuous variables were described by using mean, median, range, and interquartile range values. 
2 tests were used to compare categorical variables.
We built 2 multivariable models to address different aims. First, we fit a logistic regression model with the probability of a positive culture at different time points, including only those factors available at the time that the culture was drawn. This model was used to allow us to generate predicted probabilities for positive cultures at various time points (12, 24, 36, and 48 hours after specimen collection) based on the presence or absence of baseline factors including age, recent antibiotic use, and catheter type.
Second, we fit a Cox proportional-hazards model with the time to positivity for the blood culture by using both baseline covariates and microbiologic data. This model was used to create a more precise explanatory model to identify factors associated with the time to positivity. Time to blood-culture positivity was described by using Kaplan-Meier estimates, and the time to positivity among different groups was compared using the log-rank test. Building of the multivariable model began with inclusion of the bacterial category because of our a priori hypothesis. Age category and recent antibiotic use were included in the model as potential confounders of the association between bacterial category and time to blood-culture positivity. Other variables were considered for inclusion in the multivariable Cox proportional-hazards model if the P value was <.2; these variables remained in the final multivariable model if they were statistically significant or if their inclusion confounded the association between bacterial type and time to blood-culture positivity as defined by a >10% change in the adjusted hazard ratio (HR).15,16 Distinct episodes from the same patient were considered as separate events. However, the multivariable model was adjusted for clustering effects introduced by the inclusion of multiple episodes for individual patients. A 2-tailed P value <.05 was considered statistically significant. Global and covariate-specific tests of proportional hazards for the multivariable regression model were not significant, and, therefore, a single model was fit for the entire data set. The inclusion of 200 patients with BSIs would allow us to detect an HR for factors associated with the time to positivity of 1.5 with 80% power (
= .05) if the median time to blood-culture positivity exceeded 12 hours.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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During the study period (January 1, 2000, through December 31, 2003), blood cultures were obtained through a CVC and submitted to the Clinical Microbiology Laboratory for evaluation of 1987 episodes of suspected BSI; blood-culture results were positive in 387 episodes (19.5%). A single commensal organism was isolated from 72 episodes (18.6%) with positive blood-culture results, and these patients were excluded from the study. From the remaining 315 eligible episodes of catheter-associated bacteremia, we selected 200 episodes randomly for inclusion in this study.
Demographic data for the study patients are shown in Table 1. An absolute neutrophil count <500 per µL was present in 18% of patients. Eighteen patients (9.0%) had percutaneously inserted central catheters. The remaining catheter types included double (n = 129) or single (n = 22) lumen Broviac catheters, double-lumen Medcomp catheters (n = 12), subcutaneously implanted ports (n = 14), and other catheter types (n = 5). The catheters were in place for a median of 80.5 days (interquartile range: 33–167 days) before BSI. All of the patients had 2 blood cultures from the CVC; peripheral blood cultures were obtained from only 27 patients (14%). Thirty-six patients (18%) had experienced a BSI within the past 30 days. Ninety-six percent of the BSIs were considered primary BSIs. Pneumonia, the most common cause of secondary BSI, was diagnosed in 5 patients.
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Among the 200 study patients, 127 (63.5%) had monomicrobial infections, whereas 73 (36.5%) had polymicrobial infections. The distribution of organisms among patients with monomicrobial infections was as follows: Gram-positive bacteria (n = 69), Gram-negative bacteria (n = 50), Candida species (n = 6), and rapidly growing mycobacteria (n = 2). The most common Gram-positive bacteria causing monomicrobial infections included coagulase-negative staphylococci (n = 23), Enterococcus species (n = 9), S aureus (n = 8), and viridans group streptococci (n = 8). The most common Gram-negative bacteria causing monomicrobial infections included Pseudomonas species (n = 16) and Klebsiella species (n = 12). Among patients with polymicrobial infections, 52 (71%) included
1 Gram-negative bacillus.
The overall median time to blood-culture positivity was 14.0 hours (interquartile range: 11.1–20.4 hours). BSIs containing a Gram-negative bacillus had a shorter time to positivity than BSIs not including a Gram-negative bacillus, regardless of whether the infection was monomicrobial or polymicrobial. Of the 10 cultures that became positive after >48 hours of incubation, 3 contained a rapidly growing mycobacterium species, whereas 5 others contained skin commensals. Table 2 shows the predicted probability of a positive culture at various time points after blood-culture collection after adjusting for age category, catheter type, and recent antibiotic use. Among children with BSI, most cultures with 1 Gram-negative bacillus were positive within 24 hours of specimen collection. In contrast, the predicted probabilities were 66.4% and 84.4% at 24 and 36 hours, respectively, for BSIs caused by Gram-positive bacteria or other organisms (ie, Candida species or rapidly growing mycobacteria), whether in the context of a monomicrobial or polymicrobial infection. Figure 1 shows the time to blood-culture positivity stratified by bacterial category. The median time to positivity was as follows: polymicrobial with 1 Gram-negative bacillus, 11.2 hours; Gram-negative bacilli (monomicrobial infection), 12.8 hours; polymicrobial without any Gram-negative bacilli, 16.1 hours; Gram-positive bacteria, 19.0 hours; and other bacteria, 24.4 hours. There were no significant differences in the time to positivity between bacteria within a specific category (eg, coagulase-negative staphylococci compared with S aureus; data not shown). Polymicrobial infections containing Gram-negative bacteria had an earlier time to positivity compared with monomicrobial infections with Gram-negative bacteria (P = .042, log-rank test).
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The unadjusted analysis identifying factors associated with time to blood-culture positivity is shown in Table 3. Demographic factors such as gender, race, and comorbid medical conditions, as well as site of initial evaluation (emergency department versus subspecialty clinic) and initial disposition (immediate hospitalization versus initial discharge with subsequent hospitalization), were not associated with an earlier time to positivity on unadjusted analysis. There was no clearly discernible relationship between antibiotic class administered and time to blood-culture positivity. On multivariable analysis, BSIs caused by Gram-negative bacteria, whether in the context of a monomicrobial or polymicrobial infection, remained significantly associated with an earlier time to positivity even after adjusting for age, catheter type, and receipt of recent antibiotic therapy (Table 4).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Our study shows that, in children with CVC-associated BSIs evaluated in the ambulatory setting, the time to blood-culture positivity depends on bacterial category. BSIs caused by Gram-negative bacteria are detected most quickly, with virtually all of the cultures with Gram-negative bacteria being positive within 36 hours of specimen collection, regardless of whether they occur in the context of a monomicrobial or polymicrobial infection. Furthermore, >96% of BSIs caused by any organism are detected within 36 hours of specimen collection; additional incubation periods did not substantially increase the yield of culture after adjusting for age, catheter type, and recent antibiotic use. These data suggest that discontinuation of empiric antibiotic coverage may be warranted in clinically stable children with CVCs earlier than the traditional "48-hour rule-out" period.
Several studies have explored the time to blood-culture positivity in immunocompetent children.10–12 Alpern et al10 determined time to blood-culture positivity in children 2 to 24 months of age and found that >95% of cultures were positive within 24 hours; S pneumoniae accounted for the majority of pathogenic bacteria isolated. McGowan et al11 found that cultures were positive in 87% and 92% of 239 children with bacteremia at 24 and 36 hours, respectively, after specimen collection. However, there was considerable variability in the time to blood-culture positivity among different bacteria; >95% of all enteric Gram-negative bacteria (n = 24) were positive within 24 hours of specimen collection from children without CVCs or underlying malignancy.11 In our study, which was limited to children with CVCs, there was also variability by organism category in the time to blood-culture positivity, with most cultures containing Gram-negative bacteria having an earlier time to positivity. In contrast, 1 study of adults found a longer time to positivity compared with our study. Among adults with BSI, 69% and 91% of all Gram-negative bacteria were detected within 24- and 48-hours, respectively.17 In that study, 60% and 90% of all bacteria were detected within 24 and 48 hours, respectively. However, patients with CVCs were not considered separately. Furthermore, differences in bacterial detection systems, blood volume cultured, and comorbid disease states make this latter study less generalizable to the pediatric population.
Changes in clinical practice, use review, and reimbursement have caused significant alterations in the delivery of pediatric inpatient care. Alternatives to traditional inpatient pediatric admissions have become commonplace with the creation of observation or short-stay admission units to reduce inpatient hospitalizations for several pediatric conditions.18–24 The typical period of observation before a child would be either sent home or hospitalized ranges from 12 to 36 hours. In our study population, where 315 (16%) of 1987 evaluated children with CVCs had true BSI, a policy of routine discharge for those with negative blood-culture results after 24 hours would result in early discharge of 1817 children; 0.3% of these would return with a Gram-negative BSI, and 1.7% would return with BSI caused by any bacteria. Extending the observation period to 36 hours would result in early discharge of 1794 children; of these, 0.05% would return with Gram-negative BSI, and 0.4% would return with BSI caused by any bacteria. Although the differences in time to blood-culture positivity for Gram-negative as compared with Gram-positive bacteria have clinical relevance as illustrated, individual physicians may have different thresholds for modifying their clinical practice based on these data.
Vomiting at presentation was also independently associated with an earlier time to blood-culture positivity. There was no association between vomiting and bacterial category. The presence of vomiting may be a marker for a more severely ill patient with a higher inoculum of bacteria in their blood.
One limitation of our study is that we could not assess blood-culture volume, an indirect measure of bacterial inoculum and, therefore, a possible determinant of time to blood-culture positivity.25,26 In children, blood volumes sent for culture are often determined as a fraction of the patient's total blood volume, estimated by patient size. To adjust for potential confounding introduced by size-related differences in blood volume sent for culture, age category was included in our final multivariable model. However, it is possible that other factors potentially associated with bacterial category, such as severity of illness, were associated with both the volume of blood obtained for culture and the time to blood-culture positivity. It is not clear whether more or less blood would be sent for culture in more severely ill patients. Thus, the true magnitude of the association between organism category and time to blood-culture positivity could be either stronger or weaker than the estimates found in our study. In addition, the time to blood-culture positivity may be imprecisely measured, depending on the accuracy of the recorded blood-culture collection time. At our institution, time-stamped laboratory specimen collection forms accompany all patient specimens. Although delays between specimen ordering and collection are possible, such delays between blood-culture ordering and collection are likely to be nondifferential, because neither the organism nor the outcome is known at the time of specimen collection. Lastly, because the peripheral blood cultures are uncommonly obtained from children with CVCs, we could not accurately distinguish CVC-associated BSIs from other causes of primary BSIs, such as translocation across a compromised bowel. Blood obtained from the CVC in a patient with a CVC-associated BSI may contain a higher concentration of bacteria and, thus, lead to an earlier time to positivity.27
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CONCLUSIONS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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The time to blood-culture positivity depends on bacterial category; BSIs caused by Gram-negative bacteria are detected most quickly. Our data suggest that discontinuation of empiric antibiotic coverage may be warranted in clinically stable children with CVCs if the blood-culture results remain negative 24 to 36 hours after collection.
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ACKNOWLEDGMENTS |
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This work was supported by the Ambulatory Pediatric Association Region II Young Investigator Award (to Dr Shah) and the Center for Clinical Epidemiology Medical Student Summer Research Fellowship (to Mr Downes).
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FOOTNOTES |
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Accepted Jun 28, 2007.
Address correspondence to Samir S. Shah, MD, Children's Hospital of Philadelphia, Division of Infectious Diseases, Room 1526, North Campus, 34th Street and Civic Center Boulevard, Philadelphia, PA 19104. E-mail: shahs{at}email.chop.edu
The authors have indicated they have no financial relationships relevant to this article to disclose.
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