Int J Hematol DOI 10.1007/s12185-014-1677-9
ORIGINAL ARTICLE
A role for peripherally inserted central venous catheters in the prevention of catheter-related blood stream infections in patients with hematological malignancies Toshiro Sakai • Kyuhei Kohda • Yuichi Konuma • Yasuko Hiraoka • Yukari Ichikawa • Kaoru Ono • Hiroto Horiguchi • Ayumi Tatekoshi Kouichi Takada • Satoshi Iyama • Junji Kato
•
Received: 8 April 2014 / Revised: 10 September 2014 / Accepted: 10 September 2014 Ó The Japanese Society of Hematology 2014
Abstract Central venous catheter-related blood stream infections (CR-BSIs) are a serious complication in patients with hematological malignancies. However, it remains unclear whether there is a difference in the rate of CR-BSI associated with the conventional type of central venous catheters (cCVCs) and peripherally inserted CVCs (PICCs) in such patients. To address this question, we retrospectively investigated the incidence of CR-BSIs associated with PICCs versus cCVCs in patients with hematological malignancies. We used PICCs in all consecutive patients requiring CVC placement between February 2009 and February 2013. We compared the CR-BSI rate in patients with PICCs with that in patients with cCVCs treated between September 2006 and January 2009 (control group). Eighty-four patients received PICCs and 85 received cCVCs. The most common reason for removal due to catheter-related complications was CR-BSI. The CR-BSI rate in the PICC group was significantly lower than that in the cCVC group (PICCs: 1.23/1000 catheter days; cCVCs: 5.30/1000 catheter days; P \ 0.01). Catheter-related complications other than CR-BSIs occurred at
T. Sakai (&) K. Kohda Y. Konuma Department of Hematology and Oncology, Asahikawa Red Cross Hospital, 1-1 Akebono-cho, Asahikawa, Hokkaido, Japan e-mail: [email protected] Y. Hiraoka Y. Ichikawa Department of Infection Control and Prevention, Asahikawa Red Cross Hospital, Asahikawa, Japan K. Ono H. Horiguchi A. Tatekoshi K. Takada S. Iyama J. Kato Department of Medical Oncology and Hematology, Sapporo Medical University, Sapporo, Japan
an extremely low rate in the PICC group. The median catheter-related complication-free survival duration was significantly longer in the PICC group than in the cCVC group. Our study shows that PICCs are useful in patients with hematological malignancies. Keywords Peripherally inserted central venous catheter Hematological malignancy Catheter-related blood stream infection
Introduction Central venous catheter-related blood stream infections (CR-BSIs) are associated with significant morbidity, mortality, and expense. Patients with hematological malignancies represent a special patient group at high risk for CR-BSIs because most of them require indwelling central venous catheters (CVCs) for anti-cancer therapy, transfusion, and infusion therapy. Additionally, these patients should retain these CVCs during the neutropenic period. Peripherally inserted central venous catheters (PICCs) were first reported by Hoshal in 1975 [1] as a safer alternative to the conventional type of CVCs (cCVCs), particularly for patients in whom long-term venous access is required. PICCs have been reported to reduce the incidence of CR-BSIs in hospitalized patients in a surgical intensive care unit setting [2] and in outpatients receiving intravenous treatment at home [3]. However, there are few reports on the incidence of CR-BSIs in patients with hematological malignancies who received PICCs [4–7]. In this study, we retrospectively compared the incidence of CR-BSIs in patients with hematological malignancies who received PICCs and those who received cCVCs.
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Patients and methods Patients This study was a retrospective analysis of patients with hematological malignancies who were admitted to the Department of Hematology and Oncology, Asahikawa Red Cross Hospital between February 2009 and February 2013. During this period, we inserted PICCs into all consecutive patients who required CVC placement for therapy. We analyzed and compared the CR-BSI rate in patients who had insertion of PICCs with that of patients who had insertion of cCVCs (control group) who had been admitted to our department between September 2006 and January 2009. PICCs and cCVCs were used as venous access for chemotherapy, stem cell infusion, antibiotic agent administration, blood infusion, and blood sample collection. Methods All of the catheters were placed by experienced physicians under maximum barrier precaution. All of the PICCs were single-lumen, silicone, 4 Fr, Groshong NXT PIC catheters (Bard Access Systems, Inc., Salt Lake City, UT, USA). This catheter has a rounded, closed-ended tip with a threeway valve designed to prevent the reflux of blood into the catheter. No heparin lock was used. Catheters were flushed and locked with 20 ml of 0.9 % saline solution every 7 days. All of the PICCs were placed via ultrasound-guided venipuncture and the Seldinger technique under X-ray radioscopy. The insertion site was limited to the basilic vein of the right or left upper arm. Either the right or left arm was selected in accordance with the patient’s will. All of the cCVCs were non-tunneled, open-ended, and either single or double-lumen catheters (Sherwood Medical Company, St. Louis, MO, USA or Covidien, Mansfield, MA, USA). A heparin lock (heparinized solution, 50 U in a 5-ml volume) was used daily. The cCVC was placed at the bedside according to the Seldinger technique, and its position was verified via chest radiography prior to use. The insertion site was limited to the internal jugular or subclavian vein. However, the inguinal vein was used during emergency situations in a limited number of patients. Definitions The CR-BSI was defined according to the Infectious Disease Society of America (IDSA) Clinical Practice Guidelines for the Diagnosis and Management of Intravascular Catheter-related Infections: 2009 Update [8] as follows: bacteremia or fungemia in patients who have an intravascular device and [1 positive blood culture result obtained
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from a peripheral vein; clinical manifestations of infection (e.g., fever, chills, and/or hypotension); and no apparent source for blood stream infection (with the exception of the catheter).One of the following definitions should be present: (1) the same organism (species) was isolated from a catheter segment and peripheral blood; and (2) microbe growth was observed from the catheter hub blood sample at least 2 h before microbe growth from a peripheral vein blood sample using two collected and cultured blood samples (1 from a catheter hub and the other from a peripheral vein). Catheters were removed for either non-catheter-associated reasons or catheter-related complications. Removal for non-catheter-associated reasons was defined as follows: the end of therapy and the patient’s wish to remove the catheter because of a temporary visit to home, or death. Catheterrelated complications were defined as CR-BSI, catheter occlusion, thrombosis, or an uncontrolled exit-site infection. Data were obtained from the patients’ medical records and nurses’ checklists for infection control. Statistical analysis The primary outcome of this study was comparison of the CR-BSI rate between the cCVC and PICC groups. The CRBSI rate was calculated using the denominator ‘‘per 1000 catheter days’’ [9], and comparison of rates was performed with 95 % confidence intervals (CIs). The Student’s t test was used where applicable. A two-sided P value of \0.05 was considered significant. Furthermore, regarding the comparison of removal for catheter-related complications, we calculated the catheter-related complication-free survival duration according to the Kaplan–Meier method. We used the log-rank test to compare the differences in the duration of catheterization and frequency of removal for catheter-related complications between the cCVC and PICC groups. All analyses were performed using GraphPad Prism software, version 5 (GraphPad Inc., San Diego, CA, USA).
Results The characteristics of the patients in both groups are shown in Table 1. Eighty-four patients received PICCs and 85 received cCVCs. The cumulative total number of catheters was 101 PICCs and 148 cCVCs. Both groups were similar in terms of sex, age, and diagnosis. In the PICC group, 64 patients received hematopoietic stem cell transplantation (HSCT). Of these, 40 received autologous HSCT (autoHSCT) and 24 received allogeneic HSCT (allo-HSCT). Thirty-four patients in the cCVC group received HSCT. Of
A role for peripherally inserted central venous catheters Table 1 Patients’ characteristics PICC
CVC
P
No. of patients
84
85
No. of catheters
101
148
Sex (M/F)
53/31
54/31
0.95
Age (years) (mean ± SD)
61.0 ± 11.8
61.5 ± 14.2
0.65
ML
31
41
AML
29
23
MM
12
6
ALL
3
6
MDS
3
5
CML Other
3 3
2 2
Auto-HSCT
40
23
Allo-HSCT
24
11
Diagnosis
Fig. 1 Comparison of the CR-BSI rate between the cCVC and PICC groups. The CR-BSI rates were 1.23 per 1000 catheter days and 5.30 per 1000 catheter days in the PICC and cCVC groups, respectively. The CR-BSI rate in the PICC group was significantly lower than that in the cCVC group (P \ 0.01)
HSCT Table 2 Details of the patients who developed CR-BSI in the PICC group
Insertion site Basilic (R/L)
101 (29/72)
Subclavian
111
Jugular
26
Inguinal
11
Duration of catheterization (days) Mean ± SD
72.4 ± 63.99
28.0 ± 17.62
Range
5–318
2–91
\0.01
SD standard deviation, auto-HSCT autologous hematopoietic stem cell transplantation, allo-HSCT allogeneic hematopoietic stem cell transplantation, ML malignant lymphoma, AML acute myeloid leukemia, MM multiple myeloma, ALL acute lymphoid leukemia, MDS myelodysplastic syndrome, CML chronic myeloid leukemia, R right arm, L left arm
these, 23 patients received auto-HSCT and 11 received allo-HSCT. All of the PICCs were placed into the basilic veins. Left arm insertion was selected by 72 patients (71.3 %). The cCVCs were primarily inserted into subclavian veins (67.6 %). The 101 PICCs remained in situ for a total of 7321 catheter days. The median duration of catheterization was 53.0 days with a range of 5–318 days [mean duration: 72.4 days, standard deviation (SD): 63.99 days]. The 148 cCVCs remained in situ for a total of 4148 catheter days. The median duration of catheterization was 25.5 days with a range of 1–91 days (mean duration: 28.0 days, SD: 17.62 days), which was a shorter duration than that of the PICC group (P \ 0.01). The most common reason for removal due to catheterrelated complications was CR-BSIs. The PICC group included nine cases of CR-BSI (8.9 %) and the cCVC group included 22 cases (14.9 %). There was a significantly lower CR-BSI rate in the PICC group compared
Age (years)/ sex
Diagnosis
Therapy
Time to onset of CR-BSI (days)
Insertion site
Causative pathogens
68/M
AML
Chemo
20
Basilic
S. epidermidis
61/F
ML
AlloHSCT
43
Basilic
S. epidermidis
57/F
ML
AlloHSCT
109
Basilic
S. epidermidis
50/F
ML
Chemo
7
Basilic
S. epidermidis
50/F
AML
Chemo
9
Basilic
S. aureus
44/F
ML
Chemo
5
Basilic
S. aureus
50/F
MDS
Chemo
83
Basilic
Candida spp.
58/F
ALL
AlloHSCT
53
Basilic
S. epidermidis
55/M
AML
AlloHSCT
76
Basilic
P. aeruginosa
M male, F female, AML acute myeloid leukemia, ML malignant lymphoma, ALL acute lymphoid leukemia, chemo chemotherapy, MDS myelodysplastic syndrome, allo-HSCT allogeneic hematopoietic stem cell transplantation, S staphylococcus, P pseudomonas, spp species
with the cCVC group (P \ 0.01, Fig. 1). The CR-BSI rate in the PICC group was 1.23 per 1000 catheter days (95 % CI 1.02–1.44 per 1000 catheter days) versus 5.30 per 1000 catheter days in the cCVC group (95 % CI 4.76–5.85). Tables 2 and 3 show the details of patients who developed CR-BSIs in both groups. We calculated the mean time to onset of CR-BSI, and found that it was 33.8 days in the cCVC group (95 %CI 25.0–42.6) and 45.0 days in the PICC group (95 %CI 15.8–74.19), with no significant difference between the two groups (P = 0.27). With regard to the insertion site of catheters, all of the patients in the PICC group had insertion via the basilic vein. In the cCVC
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T. Sakai et al. Table 3 Details of the patients who developed CR-BSI in the cCVC group Age (year)/ sex
Diagnosis
57/M
ML
43/M
Therapy
Table 4 Reasons for catheter removal PICC
cCVC
86 (85.1 %)
110 (74.4 %)
Time to onset of CR-BSI (days)
Insertion site
Causative pathogens
Chemo
22
Subclavian
S. epidermidis
CR-BSI
9 (8.9 %)
ALL
Chemo
7
Subclavian
S. aureus
Occlusion
4 (4.0 %)
8 (5.4 %)
76/M
CML
Chemo
31
Subclavian
S. epidermidis
Thrombosis
0
1 (0.7 %)
46/M
MDS
AlloHSCT
54
Subclavian
S. epidermidis
Exit-site infection
2 (2.0 %)
7 (4.7 %)
83/M
AML
Chemo
15
Subclavian
Kebsiella spp.
35/F
ALL
AlloHSCT
66
Subclavian
Candida spp.
35/F
ALL
AlloHSCT
49
Subclavian
S. epidermidis
45/F
AML
Chemo
26
Subclavian
S. epidermidis
47/F
Other
Chemo
22
Jugular
P. aeruginosa
63/M
ML
AutoHSCT
8
Subclavian
S. epidermidis
57/M
AML
Chemo
48
Subclavian
S. epidermidis
60/F
AML
Chemo
17
Subclavian
S. epidermidis
35/M
AML
AlloHSCT
66
Jugular
S. aureus
53/M
ML
AutoHSCT
33
Subclavian
Enterococcus spp.
45/M
ML
Chemo
42
Subclavian
Kebsiella spp.
46/M
ML
Chemo
64
Subclavian
S. epidermidis
46/M
ML
Chemo
14
Subclavian
S. epidermidis
61/F
ALL
Chemo
11
Subclavian
S. aureus
34/F
AML
Chemo
36
Subclavian
S. epidermidis
61/M
ML
Chemo
63
Inguinal
S. epidermidis
51/M
ML
AutoHSCT
21
Subclavian
S. epidermidis
74/F
AML
Chemo
28
Jugular
S. epidermidis
Removal for non-catheter-associated reasons
Removal for catheter-related complications
M male, F female, ML malignant lymphoma, AML acute myeloid leukemia, ALL acute lymphoid leukemia, CML chronic myeloid leukemia, MDS myelodysplastic syndrome, chemo chemotherapy, auto-HSCT autologous hematopoietic stem cell transplantation, allo-HSCT allogeneic hematopoietic stem cell transplantation, S staphylococcus, P pseudomonas, spp species
22 (14.9 %)
CR-BSI catheter-related blood stream infection, cCVC conventional type of central venous catheter, PICC peripherally inserted central venous catheter
Fig. 2 Comparison of the catheter-related complication-free survival between the cCVC and PICC groups. The survival curve shows the percentage of non-removed catheters without catheter-related complications over time. Survival in the PICC group was significantly longer than that in the cCVC group (P \ 0.01)
significantly longer in the PICC than cCVC group (P \ 0.01).
Discussion group, the insertion site in the majority of patients with CR-BSIs was the subclavian vein (18/22 cases, 81.8 %). The most common causative pathogen was Staphylococcus epidermidis in both groups. The incidence of catheter removal for non-catheterassociated reasons was similar in both groups (PICC group, 85 %; cCVC group, 74.4 %; Table 4). Other minor catheter-related complications for catheter removal are shown in Table 4. Comparison of the catheter-related complication-free survival duration is shown in Fig. 2. The median catheterrelated complication-free survival duration was 63.0 days for patients in the cCVC group; the median was not reached in the PICC group. The time to onset of catheter removal because of catheter-related complications was
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Safe and reliable intravascular access is essential in the treatment of patients with hematological malignancies. The ideal device should be easily and safely placed and removed, even in neutropenic patients and patients with bleeding tendencies, should facilitate easy blood withdrawal and drug delivery, exhibit a low complication rate, and be well tolerated by the patient. Peripherally inserted central venous catheters might be a safer alternative to cCVCs because the rate of major and critical CR-BSIs tends to be lower with PICCs than with cCVCs. The CR-BSI rate among patients with PICCs has been reported to range from 0.4 to 0.8 per 1000 catheter days, although the majority of these infections occur in a low-risk outpatient setting [3, 10, 11]. One reason for the
A role for peripherally inserted central venous catheters
low CR-BSI rate associated with PICCs that are inserted in the upper arm might represent the benefits of the insertion site. Specifically, the upper arm is less colonized, less oily, and less moist than the chest wall or neck [12, 13]. There have been several reports regarding comparison of the rate of CR-BSI associated with PICCs and cCVCs in hospitalized patients in surgical care units [2, 14, 15]. Mark et al. [2] reported that PICC use was associated with a lower CR-BSI rate than that observed with cCVC use (CR-BSI rate: 2.1 per 1000 catheter days for PICCs and 6.0 per 1000 catheter days for cCVCs). However, in patients with hematological malignancies, few reports have addressed the incidence of CR-BSIs in patients with PICCs [4–7]. Moreover, comparison of the CR-BSI rate associated with PICCs and cCVCs or tunneled devices (e.g., Hickman catheter) is limited to two reports [4, 7]. Worth et al. [4] reported that there was no significant difference in a hematological population in terms of the CR-BSI rate in patients who received PICCs (75 catheters) compared with that in those who received cCVCs (31 catheters; 6.6 per 1000 catheter days in PICC versus 10.27 per 1000 catheter days in cCVCs; P = 0.78). Mollee et al. [6] determined the incidence and risk factors for CR-BSI in a prospective cohort study of 727 adult patients with solid tumors and hematological malignancies who required placement of one of the following central venous access devices: non-tunneled catheter (e.g., cCVC), tunneled catheter, implantable port, and PICC. A total of 1127 central venous access devices were assessed in 727 patients over 51514 total catheter days. In their study, significantly more CR-BSI events occurred in patients with cCVCs compared with patients with PICCs among all patients with aggressive hematological malignancies (4.22 per 1000 catheter days in PICCs versus 17.3 per 1000 catheter days in cCVCs). Bellsei et al. [5] reported a low CR-BSI rate (1.5 per 1000 catheter days) in 57 patients with hematological malignancies who underwent auto-HSCT. Recently, Lim et al. [7] presented retrospective data for the CR-BSI rate in 84 PICCs and 64 tunneled catheters (Hickman catheters) that had been placed in patients with acute myeloid leukemia who were undergoing induction chemotherapy. They showed that the CR-BSI rate was similarly low with both types of catheters (1.00 per 1000 catheter days for PICCs versus 1.88 per 1000 catheter days for Hickman catheters; P = 0.487). Our study showed that in a relatively large population of patients with hematological malignancies, PICC use resulted in a significantly lower CR-BSI rate (1.23 per 1000 catheter days) than did cCVC use (5.30 per 1000 catheter days). Accordingly, we believe that prevention of CR-BSI in patients with hematological malignancies is a benefit on the use of PICC. This low CR-BSI rate
associated with PICCs is consistent with the results reported by Bellsei et al. [5] and Lim et al. [7]. In contrast, the results reported by Worth et al. [4] and Mollee et al. [6] were different from our results regarding the CR-BSI rate associated with PICCs. One explanation for this discrepancy between studies might be because of the different definitions of CR-BSI among the studies. Bellsei et al. [5] and Lim et al. [7] defined CR-BSI according to the IDSA Clinical Practice Guidelines, similar to our study. Accordingly, our PICCassociated CR-BSI rate is similar to the results of these two reports. However, Worth et al. [4] and Mollee et al. [6] defined CR-BSI according to the National Nosocomial Infection Surveillance (NNIS) criteria. According to recent NNIS definitions, ‘‘true’’ CR-BSI is considered as different from ‘‘central line-associated bloodstream infection’’ because the NNIS criteria were designed for surveillance purposes rather than clinical management [16]. In our study, the low PICC-related complication rate compared with the cCVC-related complication rate, including CR-BSI, enabled a longer catheter-related complication-free survival duration. Other PICC-related complications, such as thrombosis and catheter occlusion, have been reported [17, 18]. These catheter-related complications were rare in our study (thrombosis 0 %, occlusion 4 %). Recently, Hatakeyama et al. [19] also reported that PICC placement provides long-term intravenous access in Japanese children suffering from malignancy because of the low catheter-related complication rate (including infection and occlusion). We consider that there are several possible reasons for the lower rate of catheter-related thrombosis in this study compared with previous reports. One reason is the use of ultrasound guidance to ensure correct catheter placement, which has been shown to minimize the risks of endothelial injury and phlebitis [17]. In addition, the choice of single-lumen and small-caliber catheters might have reduced the incidence of catheterrelated thrombosis [5]. In regard to the low rate of catheter occlusion, we chose to place PICCs that included a three-way tip valve in all patients. In previous studies, PICCs with a three-way catheter tip valve were associated with a markedly reduced incidence of removal because of the low incidence of occlusion events [19, 20]. Therefore, selection of PICCs with a single-lumen, a small-caliber, and a three-way catheter tip valve might have led to low rates of thrombosis and catheter occlusion in our study. This type of PICC might be more beneficial than cCVCs and enable reliable long-term intravenous access, such as using tunneled devices (e.g., Hickman catheters). On the other hand, the upper arm vein was difficult to identify by visual observation and we had no landmark at
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insertion. Therefore, we needed to insert a PICC using ultrasound. Considering the reason for insertion of a PICC using X-ray radioscopy, correcting catheter malposition after insertion is impossible (e.g., into the internal jugular vein). Because the catheter tip is not an open-end type, but a closed-end type instead, moving the catheter in the correct position using a guide wire is unlikely possible to proceed. Therefore, to enable catheterization in the correct position at the first insertion, we inserted a PICC using X-ray radioscopy. This inconvenience may be a disadvantage of PICCs. The PICCs and cCVCs in all of our patients were consecutively placed at a single institute. Therefore, our study, which was not prospective, has some limitations. First, since we attempted to evaluate an equal number of patients in both groups, there was a difference in the period of observation time between the two groups (4 years in the PICC group and 2 years, 4 months in the cCVC group). Although the characteristics of diagnosis were similar in both groups, the longer observation time in the PICC group caused a significantly high proportion of HSCT recipients in this group. However, HSCT recipients had a tendency for a longer duration and intensity of neutropenic episodes. The neutropenic phase represented a significantly high risk factor for patients with hematological malignancies to develop CR-BSI, and especially, HSCT was described as the one of the main significant risk factors for CR-BSI by Chaberny et al. [21]. Judging from this fact, we believe that more HSCT recipients in the PICC group did not cause a low rate of CR-BSI. Second, the maintenance period required for catheters was different between the groups, with every 7 days for PICCs and every day for cCVCs. As a result, the removal of a catheter because of a temporary visit to home was rare in the PICC group. However, because of the limitations of this study, we could not precisely collect data for removal of non-catheter-associated. In the PICC group, we believe, not only the removal for catheter-related complication was low rate, but also the difference of maintenance period required for catheter was second reasons for longer duration of catheterization. For these two reasons, when using a PICC inserted at admission, some patients are able to finish a series of therapy in safety. In conclusion, the present study shows that PICC use is associated with a reduced CR-BSI rate relative to that associated with cCVCs. PICCs provide reliable access for prolonged intravenous administration and blood sampling in patients with hematological malignancies. A randomized study will be required to validate these findings. Conflict of interest of interest.
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The authors declare that they have no conflict
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20. Abedin S, Kapoor G. Peripherally inserted central venous catheters are a good option for prolonged venous access in children with cancer. Pediatr Blood Cancer. 2008;51:251–5. 21. Chaberny IF, Ruseva E, Sohr D, Buchholz S, Ganser A, Mattner F, et al. Surveillance with successful reduction of central lineassociated bloodstream infections among neutropenic patients with hematologic or oncologic malignancies. Ann Hematol. 2009;88:907–12.
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ORIGINAL ARTICLE
A role for peripherally inserted central venous catheters in the prevention of catheter-related blood stream infections in patients with hematological malignancies Toshiro Sakai • Kyuhei Kohda • Yuichi Konuma • Yasuko Hiraoka • Yukari Ichikawa • Kaoru Ono • Hiroto Horiguchi • Ayumi Tatekoshi Kouichi Takada • Satoshi Iyama • Junji Kato
•
Received: 8 April 2014 / Revised: 10 September 2014 / Accepted: 10 September 2014 Ó The Japanese Society of Hematology 2014
Abstract Central venous catheter-related blood stream infections (CR-BSIs) are a serious complication in patients with hematological malignancies. However, it remains unclear whether there is a difference in the rate of CR-BSI associated with the conventional type of central venous catheters (cCVCs) and peripherally inserted CVCs (PICCs) in such patients. To address this question, we retrospectively investigated the incidence of CR-BSIs associated with PICCs versus cCVCs in patients with hematological malignancies. We used PICCs in all consecutive patients requiring CVC placement between February 2009 and February 2013. We compared the CR-BSI rate in patients with PICCs with that in patients with cCVCs treated between September 2006 and January 2009 (control group). Eighty-four patients received PICCs and 85 received cCVCs. The most common reason for removal due to catheter-related complications was CR-BSI. The CR-BSI rate in the PICC group was significantly lower than that in the cCVC group (PICCs: 1.23/1000 catheter days; cCVCs: 5.30/1000 catheter days; P \ 0.01). Catheter-related complications other than CR-BSIs occurred at
T. Sakai (&) K. Kohda Y. Konuma Department of Hematology and Oncology, Asahikawa Red Cross Hospital, 1-1 Akebono-cho, Asahikawa, Hokkaido, Japan e-mail: [email protected] Y. Hiraoka Y. Ichikawa Department of Infection Control and Prevention, Asahikawa Red Cross Hospital, Asahikawa, Japan K. Ono H. Horiguchi A. Tatekoshi K. Takada S. Iyama J. Kato Department of Medical Oncology and Hematology, Sapporo Medical University, Sapporo, Japan
an extremely low rate in the PICC group. The median catheter-related complication-free survival duration was significantly longer in the PICC group than in the cCVC group. Our study shows that PICCs are useful in patients with hematological malignancies. Keywords Peripherally inserted central venous catheter Hematological malignancy Catheter-related blood stream infection
Introduction Central venous catheter-related blood stream infections (CR-BSIs) are associated with significant morbidity, mortality, and expense. Patients with hematological malignancies represent a special patient group at high risk for CR-BSIs because most of them require indwelling central venous catheters (CVCs) for anti-cancer therapy, transfusion, and infusion therapy. Additionally, these patients should retain these CVCs during the neutropenic period. Peripherally inserted central venous catheters (PICCs) were first reported by Hoshal in 1975 [1] as a safer alternative to the conventional type of CVCs (cCVCs), particularly for patients in whom long-term venous access is required. PICCs have been reported to reduce the incidence of CR-BSIs in hospitalized patients in a surgical intensive care unit setting [2] and in outpatients receiving intravenous treatment at home [3]. However, there are few reports on the incidence of CR-BSIs in patients with hematological malignancies who received PICCs [4–7]. In this study, we retrospectively compared the incidence of CR-BSIs in patients with hematological malignancies who received PICCs and those who received cCVCs.
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Patients and methods Patients This study was a retrospective analysis of patients with hematological malignancies who were admitted to the Department of Hematology and Oncology, Asahikawa Red Cross Hospital between February 2009 and February 2013. During this period, we inserted PICCs into all consecutive patients who required CVC placement for therapy. We analyzed and compared the CR-BSI rate in patients who had insertion of PICCs with that of patients who had insertion of cCVCs (control group) who had been admitted to our department between September 2006 and January 2009. PICCs and cCVCs were used as venous access for chemotherapy, stem cell infusion, antibiotic agent administration, blood infusion, and blood sample collection. Methods All of the catheters were placed by experienced physicians under maximum barrier precaution. All of the PICCs were single-lumen, silicone, 4 Fr, Groshong NXT PIC catheters (Bard Access Systems, Inc., Salt Lake City, UT, USA). This catheter has a rounded, closed-ended tip with a threeway valve designed to prevent the reflux of blood into the catheter. No heparin lock was used. Catheters were flushed and locked with 20 ml of 0.9 % saline solution every 7 days. All of the PICCs were placed via ultrasound-guided venipuncture and the Seldinger technique under X-ray radioscopy. The insertion site was limited to the basilic vein of the right or left upper arm. Either the right or left arm was selected in accordance with the patient’s will. All of the cCVCs were non-tunneled, open-ended, and either single or double-lumen catheters (Sherwood Medical Company, St. Louis, MO, USA or Covidien, Mansfield, MA, USA). A heparin lock (heparinized solution, 50 U in a 5-ml volume) was used daily. The cCVC was placed at the bedside according to the Seldinger technique, and its position was verified via chest radiography prior to use. The insertion site was limited to the internal jugular or subclavian vein. However, the inguinal vein was used during emergency situations in a limited number of patients. Definitions The CR-BSI was defined according to the Infectious Disease Society of America (IDSA) Clinical Practice Guidelines for the Diagnosis and Management of Intravascular Catheter-related Infections: 2009 Update [8] as follows: bacteremia or fungemia in patients who have an intravascular device and [1 positive blood culture result obtained
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from a peripheral vein; clinical manifestations of infection (e.g., fever, chills, and/or hypotension); and no apparent source for blood stream infection (with the exception of the catheter).One of the following definitions should be present: (1) the same organism (species) was isolated from a catheter segment and peripheral blood; and (2) microbe growth was observed from the catheter hub blood sample at least 2 h before microbe growth from a peripheral vein blood sample using two collected and cultured blood samples (1 from a catheter hub and the other from a peripheral vein). Catheters were removed for either non-catheter-associated reasons or catheter-related complications. Removal for non-catheter-associated reasons was defined as follows: the end of therapy and the patient’s wish to remove the catheter because of a temporary visit to home, or death. Catheterrelated complications were defined as CR-BSI, catheter occlusion, thrombosis, or an uncontrolled exit-site infection. Data were obtained from the patients’ medical records and nurses’ checklists for infection control. Statistical analysis The primary outcome of this study was comparison of the CR-BSI rate between the cCVC and PICC groups. The CRBSI rate was calculated using the denominator ‘‘per 1000 catheter days’’ [9], and comparison of rates was performed with 95 % confidence intervals (CIs). The Student’s t test was used where applicable. A two-sided P value of \0.05 was considered significant. Furthermore, regarding the comparison of removal for catheter-related complications, we calculated the catheter-related complication-free survival duration according to the Kaplan–Meier method. We used the log-rank test to compare the differences in the duration of catheterization and frequency of removal for catheter-related complications between the cCVC and PICC groups. All analyses were performed using GraphPad Prism software, version 5 (GraphPad Inc., San Diego, CA, USA).
Results The characteristics of the patients in both groups are shown in Table 1. Eighty-four patients received PICCs and 85 received cCVCs. The cumulative total number of catheters was 101 PICCs and 148 cCVCs. Both groups were similar in terms of sex, age, and diagnosis. In the PICC group, 64 patients received hematopoietic stem cell transplantation (HSCT). Of these, 40 received autologous HSCT (autoHSCT) and 24 received allogeneic HSCT (allo-HSCT). Thirty-four patients in the cCVC group received HSCT. Of
A role for peripherally inserted central venous catheters Table 1 Patients’ characteristics PICC
CVC
P
No. of patients
84
85
No. of catheters
101
148
Sex (M/F)
53/31
54/31
0.95
Age (years) (mean ± SD)
61.0 ± 11.8
61.5 ± 14.2
0.65
ML
31
41
AML
29
23
MM
12
6
ALL
3
6
MDS
3
5
CML Other
3 3
2 2
Auto-HSCT
40
23
Allo-HSCT
24
11
Diagnosis
Fig. 1 Comparison of the CR-BSI rate between the cCVC and PICC groups. The CR-BSI rates were 1.23 per 1000 catheter days and 5.30 per 1000 catheter days in the PICC and cCVC groups, respectively. The CR-BSI rate in the PICC group was significantly lower than that in the cCVC group (P \ 0.01)
HSCT Table 2 Details of the patients who developed CR-BSI in the PICC group
Insertion site Basilic (R/L)
101 (29/72)
Subclavian
111
Jugular
26
Inguinal
11
Duration of catheterization (days) Mean ± SD
72.4 ± 63.99
28.0 ± 17.62
Range
5–318
2–91
\0.01
SD standard deviation, auto-HSCT autologous hematopoietic stem cell transplantation, allo-HSCT allogeneic hematopoietic stem cell transplantation, ML malignant lymphoma, AML acute myeloid leukemia, MM multiple myeloma, ALL acute lymphoid leukemia, MDS myelodysplastic syndrome, CML chronic myeloid leukemia, R right arm, L left arm
these, 23 patients received auto-HSCT and 11 received allo-HSCT. All of the PICCs were placed into the basilic veins. Left arm insertion was selected by 72 patients (71.3 %). The cCVCs were primarily inserted into subclavian veins (67.6 %). The 101 PICCs remained in situ for a total of 7321 catheter days. The median duration of catheterization was 53.0 days with a range of 5–318 days [mean duration: 72.4 days, standard deviation (SD): 63.99 days]. The 148 cCVCs remained in situ for a total of 4148 catheter days. The median duration of catheterization was 25.5 days with a range of 1–91 days (mean duration: 28.0 days, SD: 17.62 days), which was a shorter duration than that of the PICC group (P \ 0.01). The most common reason for removal due to catheterrelated complications was CR-BSIs. The PICC group included nine cases of CR-BSI (8.9 %) and the cCVC group included 22 cases (14.9 %). There was a significantly lower CR-BSI rate in the PICC group compared
Age (years)/ sex
Diagnosis
Therapy
Time to onset of CR-BSI (days)
Insertion site
Causative pathogens
68/M
AML
Chemo
20
Basilic
S. epidermidis
61/F
ML
AlloHSCT
43
Basilic
S. epidermidis
57/F
ML
AlloHSCT
109
Basilic
S. epidermidis
50/F
ML
Chemo
7
Basilic
S. epidermidis
50/F
AML
Chemo
9
Basilic
S. aureus
44/F
ML
Chemo
5
Basilic
S. aureus
50/F
MDS
Chemo
83
Basilic
Candida spp.
58/F
ALL
AlloHSCT
53
Basilic
S. epidermidis
55/M
AML
AlloHSCT
76
Basilic
P. aeruginosa
M male, F female, AML acute myeloid leukemia, ML malignant lymphoma, ALL acute lymphoid leukemia, chemo chemotherapy, MDS myelodysplastic syndrome, allo-HSCT allogeneic hematopoietic stem cell transplantation, S staphylococcus, P pseudomonas, spp species
with the cCVC group (P \ 0.01, Fig. 1). The CR-BSI rate in the PICC group was 1.23 per 1000 catheter days (95 % CI 1.02–1.44 per 1000 catheter days) versus 5.30 per 1000 catheter days in the cCVC group (95 % CI 4.76–5.85). Tables 2 and 3 show the details of patients who developed CR-BSIs in both groups. We calculated the mean time to onset of CR-BSI, and found that it was 33.8 days in the cCVC group (95 %CI 25.0–42.6) and 45.0 days in the PICC group (95 %CI 15.8–74.19), with no significant difference between the two groups (P = 0.27). With regard to the insertion site of catheters, all of the patients in the PICC group had insertion via the basilic vein. In the cCVC
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T. Sakai et al. Table 3 Details of the patients who developed CR-BSI in the cCVC group Age (year)/ sex
Diagnosis
57/M
ML
43/M
Therapy
Table 4 Reasons for catheter removal PICC
cCVC
86 (85.1 %)
110 (74.4 %)
Time to onset of CR-BSI (days)
Insertion site
Causative pathogens
Chemo
22
Subclavian
S. epidermidis
CR-BSI
9 (8.9 %)
ALL
Chemo
7
Subclavian
S. aureus
Occlusion
4 (4.0 %)
8 (5.4 %)
76/M
CML
Chemo
31
Subclavian
S. epidermidis
Thrombosis
0
1 (0.7 %)
46/M
MDS
AlloHSCT
54
Subclavian
S. epidermidis
Exit-site infection
2 (2.0 %)
7 (4.7 %)
83/M
AML
Chemo
15
Subclavian
Kebsiella spp.
35/F
ALL
AlloHSCT
66
Subclavian
Candida spp.
35/F
ALL
AlloHSCT
49
Subclavian
S. epidermidis
45/F
AML
Chemo
26
Subclavian
S. epidermidis
47/F
Other
Chemo
22
Jugular
P. aeruginosa
63/M
ML
AutoHSCT
8
Subclavian
S. epidermidis
57/M
AML
Chemo
48
Subclavian
S. epidermidis
60/F
AML
Chemo
17
Subclavian
S. epidermidis
35/M
AML
AlloHSCT
66
Jugular
S. aureus
53/M
ML
AutoHSCT
33
Subclavian
Enterococcus spp.
45/M
ML
Chemo
42
Subclavian
Kebsiella spp.
46/M
ML
Chemo
64
Subclavian
S. epidermidis
46/M
ML
Chemo
14
Subclavian
S. epidermidis
61/F
ALL
Chemo
11
Subclavian
S. aureus
34/F
AML
Chemo
36
Subclavian
S. epidermidis
61/M
ML
Chemo
63
Inguinal
S. epidermidis
51/M
ML
AutoHSCT
21
Subclavian
S. epidermidis
74/F
AML
Chemo
28
Jugular
S. epidermidis
Removal for non-catheter-associated reasons
Removal for catheter-related complications
M male, F female, ML malignant lymphoma, AML acute myeloid leukemia, ALL acute lymphoid leukemia, CML chronic myeloid leukemia, MDS myelodysplastic syndrome, chemo chemotherapy, auto-HSCT autologous hematopoietic stem cell transplantation, allo-HSCT allogeneic hematopoietic stem cell transplantation, S staphylococcus, P pseudomonas, spp species
22 (14.9 %)
CR-BSI catheter-related blood stream infection, cCVC conventional type of central venous catheter, PICC peripherally inserted central venous catheter
Fig. 2 Comparison of the catheter-related complication-free survival between the cCVC and PICC groups. The survival curve shows the percentage of non-removed catheters without catheter-related complications over time. Survival in the PICC group was significantly longer than that in the cCVC group (P \ 0.01)
significantly longer in the PICC than cCVC group (P \ 0.01).
Discussion group, the insertion site in the majority of patients with CR-BSIs was the subclavian vein (18/22 cases, 81.8 %). The most common causative pathogen was Staphylococcus epidermidis in both groups. The incidence of catheter removal for non-catheterassociated reasons was similar in both groups (PICC group, 85 %; cCVC group, 74.4 %; Table 4). Other minor catheter-related complications for catheter removal are shown in Table 4. Comparison of the catheter-related complication-free survival duration is shown in Fig. 2. The median catheterrelated complication-free survival duration was 63.0 days for patients in the cCVC group; the median was not reached in the PICC group. The time to onset of catheter removal because of catheter-related complications was
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Safe and reliable intravascular access is essential in the treatment of patients with hematological malignancies. The ideal device should be easily and safely placed and removed, even in neutropenic patients and patients with bleeding tendencies, should facilitate easy blood withdrawal and drug delivery, exhibit a low complication rate, and be well tolerated by the patient. Peripherally inserted central venous catheters might be a safer alternative to cCVCs because the rate of major and critical CR-BSIs tends to be lower with PICCs than with cCVCs. The CR-BSI rate among patients with PICCs has been reported to range from 0.4 to 0.8 per 1000 catheter days, although the majority of these infections occur in a low-risk outpatient setting [3, 10, 11]. One reason for the
A role for peripherally inserted central venous catheters
low CR-BSI rate associated with PICCs that are inserted in the upper arm might represent the benefits of the insertion site. Specifically, the upper arm is less colonized, less oily, and less moist than the chest wall or neck [12, 13]. There have been several reports regarding comparison of the rate of CR-BSI associated with PICCs and cCVCs in hospitalized patients in surgical care units [2, 14, 15]. Mark et al. [2] reported that PICC use was associated with a lower CR-BSI rate than that observed with cCVC use (CR-BSI rate: 2.1 per 1000 catheter days for PICCs and 6.0 per 1000 catheter days for cCVCs). However, in patients with hematological malignancies, few reports have addressed the incidence of CR-BSIs in patients with PICCs [4–7]. Moreover, comparison of the CR-BSI rate associated with PICCs and cCVCs or tunneled devices (e.g., Hickman catheter) is limited to two reports [4, 7]. Worth et al. [4] reported that there was no significant difference in a hematological population in terms of the CR-BSI rate in patients who received PICCs (75 catheters) compared with that in those who received cCVCs (31 catheters; 6.6 per 1000 catheter days in PICC versus 10.27 per 1000 catheter days in cCVCs; P = 0.78). Mollee et al. [6] determined the incidence and risk factors for CR-BSI in a prospective cohort study of 727 adult patients with solid tumors and hematological malignancies who required placement of one of the following central venous access devices: non-tunneled catheter (e.g., cCVC), tunneled catheter, implantable port, and PICC. A total of 1127 central venous access devices were assessed in 727 patients over 51514 total catheter days. In their study, significantly more CR-BSI events occurred in patients with cCVCs compared with patients with PICCs among all patients with aggressive hematological malignancies (4.22 per 1000 catheter days in PICCs versus 17.3 per 1000 catheter days in cCVCs). Bellsei et al. [5] reported a low CR-BSI rate (1.5 per 1000 catheter days) in 57 patients with hematological malignancies who underwent auto-HSCT. Recently, Lim et al. [7] presented retrospective data for the CR-BSI rate in 84 PICCs and 64 tunneled catheters (Hickman catheters) that had been placed in patients with acute myeloid leukemia who were undergoing induction chemotherapy. They showed that the CR-BSI rate was similarly low with both types of catheters (1.00 per 1000 catheter days for PICCs versus 1.88 per 1000 catheter days for Hickman catheters; P = 0.487). Our study showed that in a relatively large population of patients with hematological malignancies, PICC use resulted in a significantly lower CR-BSI rate (1.23 per 1000 catheter days) than did cCVC use (5.30 per 1000 catheter days). Accordingly, we believe that prevention of CR-BSI in patients with hematological malignancies is a benefit on the use of PICC. This low CR-BSI rate
associated with PICCs is consistent with the results reported by Bellsei et al. [5] and Lim et al. [7]. In contrast, the results reported by Worth et al. [4] and Mollee et al. [6] were different from our results regarding the CR-BSI rate associated with PICCs. One explanation for this discrepancy between studies might be because of the different definitions of CR-BSI among the studies. Bellsei et al. [5] and Lim et al. [7] defined CR-BSI according to the IDSA Clinical Practice Guidelines, similar to our study. Accordingly, our PICCassociated CR-BSI rate is similar to the results of these two reports. However, Worth et al. [4] and Mollee et al. [6] defined CR-BSI according to the National Nosocomial Infection Surveillance (NNIS) criteria. According to recent NNIS definitions, ‘‘true’’ CR-BSI is considered as different from ‘‘central line-associated bloodstream infection’’ because the NNIS criteria were designed for surveillance purposes rather than clinical management [16]. In our study, the low PICC-related complication rate compared with the cCVC-related complication rate, including CR-BSI, enabled a longer catheter-related complication-free survival duration. Other PICC-related complications, such as thrombosis and catheter occlusion, have been reported [17, 18]. These catheter-related complications were rare in our study (thrombosis 0 %, occlusion 4 %). Recently, Hatakeyama et al. [19] also reported that PICC placement provides long-term intravenous access in Japanese children suffering from malignancy because of the low catheter-related complication rate (including infection and occlusion). We consider that there are several possible reasons for the lower rate of catheter-related thrombosis in this study compared with previous reports. One reason is the use of ultrasound guidance to ensure correct catheter placement, which has been shown to minimize the risks of endothelial injury and phlebitis [17]. In addition, the choice of single-lumen and small-caliber catheters might have reduced the incidence of catheterrelated thrombosis [5]. In regard to the low rate of catheter occlusion, we chose to place PICCs that included a three-way tip valve in all patients. In previous studies, PICCs with a three-way catheter tip valve were associated with a markedly reduced incidence of removal because of the low incidence of occlusion events [19, 20]. Therefore, selection of PICCs with a single-lumen, a small-caliber, and a three-way catheter tip valve might have led to low rates of thrombosis and catheter occlusion in our study. This type of PICC might be more beneficial than cCVCs and enable reliable long-term intravenous access, such as using tunneled devices (e.g., Hickman catheters). On the other hand, the upper arm vein was difficult to identify by visual observation and we had no landmark at
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insertion. Therefore, we needed to insert a PICC using ultrasound. Considering the reason for insertion of a PICC using X-ray radioscopy, correcting catheter malposition after insertion is impossible (e.g., into the internal jugular vein). Because the catheter tip is not an open-end type, but a closed-end type instead, moving the catheter in the correct position using a guide wire is unlikely possible to proceed. Therefore, to enable catheterization in the correct position at the first insertion, we inserted a PICC using X-ray radioscopy. This inconvenience may be a disadvantage of PICCs. The PICCs and cCVCs in all of our patients were consecutively placed at a single institute. Therefore, our study, which was not prospective, has some limitations. First, since we attempted to evaluate an equal number of patients in both groups, there was a difference in the period of observation time between the two groups (4 years in the PICC group and 2 years, 4 months in the cCVC group). Although the characteristics of diagnosis were similar in both groups, the longer observation time in the PICC group caused a significantly high proportion of HSCT recipients in this group. However, HSCT recipients had a tendency for a longer duration and intensity of neutropenic episodes. The neutropenic phase represented a significantly high risk factor for patients with hematological malignancies to develop CR-BSI, and especially, HSCT was described as the one of the main significant risk factors for CR-BSI by Chaberny et al. [21]. Judging from this fact, we believe that more HSCT recipients in the PICC group did not cause a low rate of CR-BSI. Second, the maintenance period required for catheters was different between the groups, with every 7 days for PICCs and every day for cCVCs. As a result, the removal of a catheter because of a temporary visit to home was rare in the PICC group. However, because of the limitations of this study, we could not precisely collect data for removal of non-catheter-associated. In the PICC group, we believe, not only the removal for catheter-related complication was low rate, but also the difference of maintenance period required for catheter was second reasons for longer duration of catheterization. For these two reasons, when using a PICC inserted at admission, some patients are able to finish a series of therapy in safety. In conclusion, the present study shows that PICC use is associated with a reduced CR-BSI rate relative to that associated with cCVCs. PICCs provide reliable access for prolonged intravenous administration and blood sampling in patients with hematological malignancies. A randomized study will be required to validate these findings. Conflict of interest of interest.
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The authors declare that they have no conflict
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