Abstract
Cultures taken from the skin and from the hubs of short-term central venous catheters can help us to predict catheter-related bloodstream infections (C-RBSIs). The value of these cultures for such predictions has not been assessed in long-term catheters. Our objective was to assess the value of superficial cultures for the prediction of C-RBSI among patients with long-term catheters. Over a 2-year period, we prospectively obtained cultures from the skin overlying reservoir ports (group A) and from the skin insertion site and hubs of all tunneled catheters (group B). This routine was performed by vascular and interventional radiologists immediately before catheter removal (irrespective of the reason for withdrawal). Swabs were processed semiquantitatively. Catheter tips from both groups were cultured using Maki's semiquantitative technique and sonication. We also performed cultures of the reservoir ports at different sites. C-RBSI was defined as the isolation of the same species of microorganism(s) both in the colonized catheter and in at least 1 peripheral blood culture. We included 372 catheters (group A, 223; group B, 149) during the study period. The catheter colonization rate was 23.4% (87/372), and 28 patients had C-RBSI. Validity index values for the capacity of surface cultures to predict C-RBSI in groups A and B were, respectively, as follows: sensitivity, 23.5% and 45.5%; specificity, 59.7% and 63.0%; positive predictive value, 4.6% and 8.9%; and negative predictive value, 90.4% and 93.5%. Superficial cultures of patients with long-term catheters could help us to rule out the catheter as the portal of entry of bloodstream infections. Superficial cultures (from skin and hubs) proved to be a useful conservative diagnostic tool for ruling out C-RBSI among patients with long-term tunneled catheters and totally implantable venous access ports.
INTRODUCTION
Catheter-related bloodstream infection (C-RBSI) is an important nosocomial entity with high rates of morbidity and mortality (1–5). Patients undergoing chemotherapy or hemodialysis are at risk of developing C-RBSI, as they need a permanent intravascular device. Although C-RBSI rates are low in these patients (6–12), the difficulties and complications attributable to catheter replacement require the use of alternative diagnostic tools which allow us to predict infection without having to withdraw the catheter.
Microorganisms colonizing skin, hubs, or both are considered the first step to catheter tip colonization and, consequently, to C-RBSI (13–15). Therefore, superficial cultures (skin and hubs) are good diagnostic tools for predicting catheter colonization and C-RBSI. However, they have been tested only in patients with short-term central venous catheters, who are mainly admitted to intensive care units (13, 16). Data on the usefulness of superficial cultures in a subpopulation using long-term catheters are scarce.
The purpose of our study was to assess the validity values of superficial cultures for the prediction of C-RBSI in patients with long-term tunneled catheters and totally implantable venous access ports.
MATERIALS AND METHODS
Setting.
We performed a prospective study between July 2009 and April 2011 at a large tertiary institution in Madrid, Spain.
We included all long-term central venous catheters that were routinely removed in the Vascular and Interventional Radiology Department, irrespective of the reason for withdrawal. No antimicrobial-coated catheters were used during the study period.
Catheters were classified into two groups: group A, totally implantable venous access ports; and group B, tunneled central venous catheters.
Laboratory procedures.
Catheter tips from groups A and B were analyzed using Maki's semiquantitative roll-plate technique and the sonication method in a random order (1:1). The roll-plate technique was applied by transferring each catheter tip to a plate with Columbia agar supplemented with 5% sheep blood and rolling the tip back and forth across the surface at least 3 to 4 times (17). Sonication was performed by placing the catheter tip in 10 ml of brain heart infusion broth, sonicating for 1 min (at 55,000 Hz and 125 W), and vortexing for 15 s. Then, 0.1 ml of the sonicated broth and 0.1 ml of a 1:100 dilution of the broth were streaked onto sheep blood agar plates. The plates were incubated aerobically for 48 h at 37°C. The colonies recovered were counted (18).
We performed venous access port cultures (Columbia blood agar) using the following samples and sites: port content aspirate before and after sonication, port sonication fluid, and port internal surface biofilm. The laboratory management of venous access port sites was as described in a previous study by our group (19).
The microorganisms recovered from catheter cultures were fully identified by standard microbiologic methods using an automated MicroScan system with POS Combo Panel Type 2S and NEG Combo Panel Type 1S (Dade Behring, Sacramento, CA).
Superficial cultures.
Cultures from the skin insertion site (groups A and B) and all hubs (group B) were collected immediately before catheter withdrawal. For skin samples, a dry cotton swab was rubbed over a 2-cm2 area around the insertion site. For hub samples, an alginate swab was introduced in each hub and rubbed 3 times against the inner surface. When swabs arrived at the laboratory, they were rubbed onto Columbia blood agar and incubated aerobically for 48 h at 37°C. The colonies recovered were counted. Cultures with ≥15 CFU/plate were considered positive (13). The microorganisms recovered from cultures were identified by their phenotypic characteristics.
Definitions. (i) Tunneled catheter colonization.
Tunneled catheter colonization was defined as detection of the presence of a positive semiquantitative tip culture by either the roll-plate technique (≥15 CFU/plate) or the sonication method (≥100 CFU/plate) (20).
(ii) Venous access port colonization.
Venous access port colonization was defined as detection of the presence of a positive semiquantitative tip culture by either the roll-plate technique (≥15 CFU/plate) or the sonication method (≥100 CFU/plate) and/or a positive quantitative culture (≥100 CFU/ml) of port content aspirate before or after sonication or of port sonication fluid or a positive qualitative culture of port internal surface biofilm.
(iii) Gold standard for C-RBSI.
The gold standard for C-RBSI detection was defined as isolation of the same microorganism(s) in both the colonized catheter and at least 1 peripheral blood culture obtained 7 days before or after catheter withdrawal (21).
Statistical analysis.
Qualitative variables are expressed as a frequency distribution and quantitative variables as means and standard deviations or median and interquartile ranges (nonnormal distribution).
Validity values were defined as follows: sensitivity, proportion of colonized catheters causing C-RBSI detected using the tested culture with respect to the total number of colonized catheters causing C-RBSI detected by the gold standard; specificity, proportion of noncolonized catheters not causing C-RBSI detected using the tested culture with respect to the total noncolonized catheters not causing C-RBSI detected by the gold standard; positive predictive value, proportion of colonized catheters causing C-RBSI detected using the tested culture matching colonized catheters causing C-RBSI detected by the gold standard with respect to the total colonized catheters causing C-RBSI detected by the tested culture; negative predictive value, proportion of noncolonized catheters not causing C-RBSI detected using the tested culture matching noncolonized catheters not causing C-RBSI detected by the gold standard with respect to the total noncolonized catheters not causing C-RBSI detected by the tested culture.
Statistical significance was set at P ≤ 0.05.
The statistical analysis was performed using SPSS 16.0 and EPIDAT.
Ethics.
The study was approved by the local ethics committee.
RESULTS
We included 372 long-term central venous catheters from 360 patients during the study period. Of these, 223 (59.9%) were venous access ports and 149 (40.1%) were tunneled catheters. The median catheter indwelling time was 270 days (interquartile range [IQR], 83.25 to 622.50). The main underlying disease was cancer (83.9%), followed by renal failure (16.1%). Most catheters were removed because of end of use (59.1%), followed by suspicion of bloodstream infection (22.6%). Other patient and catheter characteristics are detailed in Table 1.
Table 1.
Patient and catheter characteristicsa
| Characteristic | Value(s) |
||
|---|---|---|---|
| Overall | Group A | Group B | |
| No. of patients | 360 | 222 (61.7) | 138 (38.3) |
| Median age (IQR) in yr | 56.19 (0–87) | 54.27 (18.06) | 58.2 (16–87) |
| Male | 167 (44.9) | 90 (40.5) | 73 (52.9) |
| Underlying disease | |||
| Cancer | 303 (83.9) | 223 (100) | 80 (58.0) |
| Renal failure | 58 (16.1) | 0 (0.0) | 58 (42.0) |
| Cumulative no. of days of catheter use | 164,582 | 139,120 | 25,462 |
| Median (IQR) no. of days of catheter use | 270 (83.25–622.50) | 440 (212–907) | 137 (59–237) |
| Median (IQR) no. of times of catheter use | 20 (0.0–50.0) | 20 (1.75–50.0) | 40 (20–72) |
| Type of catheter | |||
| Port-A-Cath | 223 (59.9) | 223 (100) | 0 (0.0) |
| Hickman | 89 (23.9) | 0 (0.0) | 89 (59.7) |
| Permcath | 60 (16.1) | 0 (0.0) | 60 (40.3) |
| Site of catheter insertion | |||
| Jugular vein | 335 (90.1) | 202 (90.6) | 133 (89.3) |
| Subclavian vein | 37 (9.9) | 21 (9.4) | 16 (10.7) |
| Reason for catheter withdrawal | |||
| End of use | 220 (59.1) | 135 (60.5) | 85 (57.0) |
| Suspicion of bloodstream infection | 84 (22.6) | 44 (19.7) | 40 (26.8) |
| Suspicion of local infection | 37 (9.9) | 22 (9.9) | 15 (10.1) |
| Obstruction-malfunction | 22 (5.9) | 15 (6.7) | 7 (4.7) |
| Thrombosis | 6 (1.6) | 4 (1.8) | 2 (1.3) |
| Other | 3 (0.8) | 3 (1.3) | 0 (0.0) |
| Appearance of insertion site | |||
| Intact | 316 (84.9) | 192 (86.1) | 124 (83.2) |
| Swollen | 42 (11.3) | 18 (8.1) | 24 (16.1) |
| Ulcerated | 11 (3.0) | 10 (4.5) | 1 (0.7) |
| Suppurative | 3 (0.8) | 3 (1.3) | 0 (0.0) |
| Catheter colonization | 87 (23.4) | 48 (21.5) | 39 (26.2) |
| Microorganisms isolated in colonized catheters | |||
| Gram-positive bacteria | 78 (72.9) | 44 (74.6) | 34 (70.8) |
| Gram-negative bacteria | 18 (16.8) | 8 (13.6) | 10 (20.8) |
| Yeasts | 11 (10.3) | 7 (11.9) | 4 (8.3) |
| Total | 107 | 59 | 48 |
Values represent numbers (%) of patients except where otherwise indicated. Group A, totally implantable venous access ports; group B, long-term tunneled catheters; IQR, interquartile range.
The overall catheter colonization rate was 23.4% (87/372), and the distribution of the isolated microorganisms was as follows: Gram-positive bacteria, 72.9%; Gram-negative bacteria, 16.8%; and yeast species, 10.3% (Table 1).
During the total of 164,582 cumulative catheter days, we found 28 episodes of C-RBSI (incidence density, 0.17 episodes/1,000 catheter days). The main underlying disease with C-RBSI was cancer (78.6%), and many patients showed no external signs of infection (42.9%). The microorganisms isolated from the C-RBSI episodes were distributed as follows: Gram-positive bacteria, 62.1%; Gram-negative bacteria, 24.1%; and yeast species, 13.8%. The most frequently isolated microorganism causing C-RBSI was Staphylococcus aureus (31.0%) (Table 2).
Table 2.
Description of the 28 C-RBSI episodesa
| Characteristic | Value(s) |
||
|---|---|---|---|
| Overall | Group A | Group B | |
| No. of C-RBSI episodes | 28 | 17 (60.7) | 11 (39.3) |
| Median (IQR) age in yr | 59.28 (47.03–67.86) | 55.05 (18.75) | 59.8 (42.5–68.6) |
| Male | 15 (53.6) | 11 (64.7) | 4 (36.4) |
| Underlying disease | |||
| Cancer | 22 (78.6) | 17 (100) | 5 (45.5) |
| Renal failure | 6 (21.4) | 0 (0.0) | 6 (54.5) |
| Median (IQR) Charlson comorbidity index | 4 (2–5.75) | 5 (2.0–7.5) | 4 (2–5) |
| Mean (SD) McCabe-Jackson index | 2.68 (0.670) | 2.59 (0.712) | 2.82 (0.603) |
| Cumulative no. of days of catheter use | 13,838 | 12,303 | 1,535 |
| Median (IQR) no. of days of catheter use | 248 (55.75–726.75) | 613 (163.50–1,082.50) | 119.5 (37.8–246.3) |
| Site of catheter insertion | |||
| Jugular vein | 24 (85.7) | 13 (76.5) | 11 (100) |
| Subclavian vein | 4 (14.3) | 4 (23.5) | 0 (0.0) |
| Time that blood cultures were drawn | |||
| Before catheter withdrawal | 25 (89.3) | 15 (88.2) | 10 (90.9) |
| At catheter withdrawal | 1 (3.6) | 0 (0.0) | 1 (9.1) |
| After catheter withdrawal | 2 (7.1) | 2 (11.8) | 0 (0.0) |
| Reason for catheter withdrawal | |||
| Suspicion of bloodstream infection | 23 (82.1) | 13 (76.5) | 10 (90.9) |
| Suspicion of local infection | 5 (17.9) | 4 (23.5) | 1 (9.1) |
| Appearance of insertion site | |||
| Intact | 12 (42.9) | 5 (29.4) | 7 (63.6) |
| Ulcerated | 6 (21.4) | 6 (35.3) | 0 (0.0) |
| Swollen | 8 (28.6) | 4 (23.5) | 4 (36.4) |
| Suppurative | 2 (7.1) | 2 (11.8) | 0 (0.0) |
| Median (IQR) DDDs | 23.85 (10.63–55.50) | 29.4 (18.05–63.20) | 11 (4.80–50.00) |
| Median (IQR) total days of therapy | 16 (10.25–27.75) | 19 (14–28) | 16 (6–27) |
| Microorganisms causing C-RBSI | |||
| Gram-positive bacteria | 18 (62.1) | 11 (61.1) | 7 (63.6) |
| Staphylococcus aureus | 9 (31.3) | 6 (33.3) | 3 (27.3) |
| Staphylococcus epidermidis | 7 (24.1) | 3 (16.7) | 4 (36.4) |
| Enterococcus faecalis | 2 (6.9) | 2 (11.1) | 0 (0.0) |
| Gram-negative bacteria | 7 (24.1) | 4 (22.2) | 3 (27.3) |
| Stenotrophomonas maltophilia | 2 (6.9) | 0 (0.0) | 2 (18.2) |
| Proteus mirabilis | 2 (6.9) | 1 (5.6) | 1 (9.1) |
| Escherichia coli | 1 (3.4) | 1 (5.6) | 0 (0.0) |
| Enterobacter cloacae | 1 (3.4) | 1 (5.6) | 0 (0.0) |
| Serratia marcescens | 1 (3.4) | 1 (5.6) | 0 (0.0) |
| Yeasts | 4 (13.8) | 3 (16.7) | 1 (9.1) |
| Candida parapsilosis | 2 (6.9) | 2 (11.1) | 0 (0.0) |
| Candida glabrata | 1 (3.4) | 1 (5.6) | 0 (0.0) |
| Candida tropicalis | 1 (3.4) | 0 (0.0) | 1 (9.1) |
| Total | 29 | 18 | 11 |
Values represent numbers (%) of patients except where otherwise indicated. C-RBSI, catheter-related bloodstream infection, IQR, interquartile range; SD, standard deviation; DDDs, defined daily doses; Group A, totally implantable venous access ports; group B, long-term tunneled catheters.
The colonization rates of superficial cultures were 39.0% (86/223) and 37.6% (56/149) in groups A and B, respectively. The most predominant microorganisms were coagulase-negative staphylococci (66.7% in group A and 65.4% in group B) (Table 3). The validity values of superficial cultures for prediction of C-RBSI in groups A and B were, respectively, as follows: sensitivity, 23.5% and 45.5%; specificity, 59.7% and 63.0%; positive predictive value, 4.6% and 8.9%; and negative predictive value, 90.4% and 93.5% (Table 4).
Table 3.
Etiology of positive superficial culturesa
| Microorganism | Value(s) |
|||
|---|---|---|---|---|
| Group A (skin) | Group B |
|||
| Global | Skin | Hubs | ||
| Gram-positive bacteria | 133 (92.4) | 68 (84.0) | 67 (87.0) | 1 (25.0) |
| CoNS | 96 (66.7) | 53 (65.4) | 52 (67.5) | 1 (25.0) |
| Corynebacterium spp. | 15 (10.4) | 5 (6.2) | 5 (6.5) | 0 (0.0) |
| Staphylococcus aureus | 13 (9.0) | 9 (11.1) | 9 (11.7) | 0 (0.0) |
| Micrococcus spp. | 5 (3.5) | 1 (1.2) | 1 (1.3) | 0 (0.0) |
| Enterococcus spp. | 3 (2.1) | 0 (0.0) | 0 (0.0) | 0 (0.0) |
| Streptococcus viridans | 1 (0.7) | 0 (0.0) | 0 (0.0) | 0 (0.0) |
| Gram-negative bacteria | 10 (6.9) | 7 (8.6) | 6 (7.8) | 1 (25.0) |
| Enterobacteriaceae | 4 (2.8) | 5 (6.2) | 4 (5.2) | 1 (25.0) |
| NFGNB | 6 (4.2) | 2 (2.5) | 2 (2.6) | 0 (0.0) |
| Yeasts | 1 (0.7) | 6 (7.4) | 4 (5.2) | 2 (50.0) |
| Candida albicans | 0 (0.0) | 2 (2.5) | 1 (1.3) | 1 (25.0) |
| Candida parapsilosis | 1 (0.7) | 2 (2.5) | 2 (2.6) | 0 (0.0) |
| Candida glabrata | 0 (0.0) | 2 (2.5) | 1 (1.3) | 1 (25.0) |
| Total | 144 | 81 | 77 | 4 |
Values represent numbers (%) of patients except where otherwise indicated. CoNS, coagulase-negative staphylococci; NFGNB, nonfermenting Gram-negative bacilli; Group A, totally implantable venous access ports; group B, long-term tunneled catheters.
Table 4.
Validity values of superficial cultures for the prediction of catheter-related bloodstream infectiona
| Group | Parameter | Value (%) |
||
|---|---|---|---|---|
| Overall | Skin | Hubs | ||
| A | S | 23.5 | ||
| SP | 59.7 | |||
| PPV | 4.6 | |||
| NPV | 90.4 | |||
| B | S | 45.5 | 36.4 | 18.2 |
| SP | 63.0 | 63.8 | 98.6 | |
| PPV | 8.9 | 7.4 | 50.0 | |
| NPV | 93.5 | 92.6 | 93.8 | |
S, sensitivity; SP, specificity; PPV, positive predictive value; NPV, negative predictive value; group A, totally implantable venous access ports; group B, long-term tunneled catheters. Values of >90% are shown in boldface type.
In group B (patients with tunneled catheters), catheter hub cultures proved to have good (98.6%) specificity for the prediction of C-RBSI.
DISCUSSION
Our study showed that negative superficial cultures allow us to rule out C-RBSI in patients with long-term catheters. Long-term central venous catheters are widely used in patients with cancer or renal failure, as these populations need a permanent vascular access for chemotherapy and hemodialysis. Therefore, they are at risk of developing C-RBSI. Rates of C-RBSI range from 0.10 to 0.37 episodes/catheter days among patients undergoing chemotherapy and 0.5 to 7.6 episodes/1,000 catheter days among patients undergoing hemodialysis (6–8, 11, 22–27).
The most appropriate procedure for confirming an episode of C-RBSI is microbiological culture, which requires the catheter to be withdrawn (20). However, in this subpopulation of patients, catheter replacement is not always possible, since it involves severe complications during the surgical insertion procedure (28–30). Therefore, conservative methods may be required for the diagnosis of C-RBSI. Evaluation of differential times to positivity (DTTP) has proven effective for the diagnosis of C-RBSI in the general population (16, 31–33). However, it requires drawn blood from all catheter hubs and from a peripheral vein, which in most cases represents a great amount of blood. This, particularly, represents a big problem in the neonatal population and in patients whose catheters have persistent occlusion. Moreover, the application of DTTP evaluation for catheter-related candidemia has not been already established (34, 35). Therefore, the use of a rapid and easy-to-perform technique such as superficial culture analysis may allow us to solve these problems.
Superficial culture analyses have proven to be useful diagnostic methods that do not require the catheter to be withdrawn, as they are performed by taking cultures from the skin around the catheter insertion site and from the internal surface of all hubs (superficial cultures). However, studies evaluating this method have been tested mainly in critical ill patients with short-term central venous catheters (13, 16). We provide novel data regarding the validity values of superficial cultures tested in patients with long-term catheters. We demonstrate that superficial cultures had a good (93.5%) negative predictive value for C-RBSI in long-term catheters and could help us to rule out the catheter as the origin of the bacteremia without needing to remove it. Moreover, long-term catheters are colonized mainly by the intraluminal route (36), and our data showed that hub cultures from tunneled catheters had high (98.6%) specificity for predicting C-RBSI. This may enable C-RBSIs to be managed by combining systemic and lock antimicrobial therapy, thus obviating the need for catheter withdrawal.
The main limitations of our study were the low number of C-RBSI episodes and that we performed only superficial cultures before catheter withdrawal. Besides, we have no data available regarding antibiotic use before catheter withdrawal, which could partially explain the low sensitivity and the low positive predictive value. Moreover, our results may not be entirely applicable to all patients with long-term tunneled catheters or port reservoirs, as we did not include patients whose device was removed because of failure of conservative treatment. Future studies must evaluate the validity of superficial cultures while the catheter is being used as a surveillance measure.
In conclusion, superficial cultures performed on long-term central venous catheters may be useful for ruling out an episode of C-RBSI.
ACKNOWLEDGMENTS
This study was supported by Ministerio de Sanidad y Consumo (Instituto de Salud Carlos III) and Fundación para la Investigación Biomédica del Hospital General Gregorio Marañón (FIBHGM) (CM09/00028). This study was partially financed by grants from Fundación Mutua Madrileña de Madrid.
We thank Thomas O'Boyle for his help in the preparation of the manuscript.
We thank the members of the GEIDI Study Group for their contribution to the work as follows: José Eugenio Guerrero, Milagros Sancho, Braulio de la Calle, Carlos Sotillo, Guiomar Sánchez, Esther Bermejo López, Lorenzo Fernández Quero, Ana Lajara, Isabel Frías, Carmen Heras, María Jesús Pérez, José Maria Barrio, Alejandro Garrido Sanchez, Patricia Muñoz, Marta Rodríguez-Créixems, Mar Santos, Eduardo Verde, Fernando González García, Emilia Bastida, Maite López Gil, Teresa Blanco, Cristina Cuerda, Laura Frías, José María Tellado, Antonio Echenagusia, Fernando Camúñez, Gracia Rodríguez Rosales, Gonzalo Simó, Mikel Echenagusia, Sonia Zamorano Caballero, Ana Barrientos Guerrero, Abilio Calderón Martín, Carmen Flores Sánchez, M. Jesús Ruano Sta. Engracia, Esperanza Arranz García, M. Ana Luna Caballero, Mar San Segundo Sánchez, Amelia V. Fernández Alonso, and M. Nieves Moro Tejedor.
We declare that we have no conflicts of interest.
Footnotes
Published ahead of print 12 July 2013
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