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Ann Thorac Surg 2001;72:725-730
© 2001 The Society of Thoracic Surgeons

Original article: cardiovascular

Nosocomial bloodstream infections in patients with implantable left ventricular assist devices

Steven M. Gordon, MDa, Steven K. Schmitt, MDa, Micah Jacobs, BSa, Nicolas M. Smedira, MDb, Marlene Goormastic, MPHc, Michael K. Banbury, MDb, Mike Yeager, RNb, Janet Serkey, RNd, Katherine Hoercher, RNb, Patrick M. McCarthy, MDb

a Department of Infectious Disease, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
b Department of Cardiothoracic Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
c Transplant Center, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
d Department of Infection Control and Epidemiology, The Cleveland Clinic Foundation, Cleveland, Ohio, USA

Accepted for publication May 16, 2001.

Address reprint requests to Dr McCarthy, Department of Cardiothoracic Surgery, Kaufman Center For Heart Failure, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, Ohio 44195
e-mail: mccartp{at}ccf.org


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Implantable left ventricular assist devices (LVAD) are used as a bridge to transplantation but are associated with a high risk of infection including nosocomial bloodstream infections (BSI).

Methods. We retrospectively reviewed the medical records of all patients with implantable LVAD at the Cleveland Clinic with 72 hours or longer of LVAD support from January 1992 through June 2000, to determine the attack rate, incidence, and impact of nosocomial BSI in patients with LVAD. A nosocomial BSI was defined using Centers for Disease Control and Prevention definition. An LVAD-related BSI was defined as one where the same pathogen is cultured from the device and the blood with no other obvious source. Two hundred fourteen patients were included in the study (17,831 LVAD-days).

Results. One hundred forty BSI were identified in 104 patients for an attack rate of 49% and incidence of 7.9 BSI per 1000 LVAD-days. Thirty-eight percent of the BSI were LVAD associated. The most common pathogens causing BSI were coagulase-negative staphylococci (n = 33), Staphylococcus aureus, and Candida spp. (19 each), and Pseudomonas aeruginosa (16 each). A Cox proportional hazard model found BSI in patients with LVAD to be significantly associated with death (hazard ratio = 4.02, p < 0.001). Fungemia had the highest hazard ratio (10.9), followed by gram-negative bacteremia (5.1), and gram-positive bacteremia (2.2).

Conclusions. Patients with implantable LVAD have a high incidence of BSI, which are associated with a significantly increased mortality. Strategies for prevention of infection in LVAD recipients should focus on the drive line exit site until technical advances can achieve a totally implantable device.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Implantable left ventricular assist devices (LVAD) have been introduced as a bridge to cardiac allotransplantation, addressing the need to provide cardiovascular support for patients with end-stage heart failure [1]. There are two types of implantable LVAD currently approved by the Food and Drug Administration (HeartMate, ThermoCardiosystems [TCI], Woburn, MA, and Novacor, World Heath, Inc, Oakland, CA). Both are electrical pulsatile devices, implanted through a median sternotomy with an inflow cannula in the apex of the left ventricle and an outflow tube anastomosed to the ascending aorta. A single drive line containing the electrical cable and the atmospheric air vent leads transcutaneously from the implanted pump to the power pack outside.

Recipients of these implantable LVAD are prone to device-related infections primarily because the extracorporeal drive lines (13.5 to 15 mm in diameter) breaches the normal cutaneous defenses against infection, providing a portal of entry for potential pathogens [2, 3]. The incidence of infection increases with duration of LVAD support, (a mean of 120 days for LVAD patients awaiting heart transplantation at the Cleveland Clinic in 1999). The primary objectives of this study were to determine the attack rate and incidence of nosocomial bloodstream infections (BSI) in patients with LVAD.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Patient population
All patients undergoing an implantable LVAD at the Cleveland Clinic Foundation between January 1, 1992 and June 30, 2000, were included in the study. Patients were excluded if the duration of LVAD support was 72 hours or longer. If a patient received more than one LVAD, only the time of support on the initial device was included.

Data collection
Demographic, clinical, and microbiologic data were retrospectively abstracted from patient charts, pathology reports, and microbiology reports. During the study time period three types of LVAD were implanted in patients by cardiothoracic surgeons at the Cleveland Clinic Foundation: (1) the pneumatic HeartMate 1000 IP air-driven system (TCI); (2) the portable, vented, electrically powered HeartMate VE; and (3) the portable programmable Novacor (World Heath). In most patients the devices were implanted in a preperitoneal pocket on top of the posterior rectus sheath and below the rectus muscle [4].

Case definitions
A nosocomial BSI was defined using criteria from the Centers for Disease Control and Prevention [5]. An LVAD-associated BSI was defined as one where the same pathogen is cultured from purulent drainage around any portion of the device, including drive lines, and the blood with no other obvious source.

Case ascertainment
A computerized database of all LVAD recipients including preoperative, perioperative, and postoperative information is maintained in the Transplant Center at the Cleveland Clinic Foundation. This list was cross-referenced with a computerized database of all nosocomial BSI maintained by the Department of Infection Control and Healthcare Epidemiology.

Statistical analysis
Estimates of infection-free time by type of LVAD device were determined using Kaplan-Meier curves. The impact of BSI on death on device (all patients) and survival to transplantation were assessed using these methods. Two Cox proportional hazards models were run for time until death on device. The occurrence of a BSI was treated as a time-dependent covariate. Infection is set to zero until the model is estimating at a time point after the infection occurred, at which time infection was set to one. Probability values were considered significant if less than 0.05.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
A total of 236 LVAD were implanted in 226 patients at the Cleveland Clinic between January 1992 and June 30, 2000. Twelve patients had less than 72 hours of LVAD support and 8 patients had more than one device implanted. Therefore, 214 patients with 214 LVAD were included in the 8.5-year study period (17,831 LVAD-days). The mean age of patients was 50 years and LVAD recipients were predominately male (90%) and white (90%).

Almost all (97%) LVADs were implanted as a bridge to transplantation. The most common type of LVAD implanted was the HeartMate VE, 41% (88 patients) followed by the pneumatic HeartMate 1000 IP, 33% (70), and the Novocar device, 26% (56 patents). We identified a total of 140 nosocomial BSI in 104 patients, for an attack rate of 49% and incidence of 7.9 BSI per 1000 LVAD-days. Thirty-eight percent (53 patients) of these BSI were LVAD associated; other sources for BSI in these patients included vascular catheters (16%), lower respiratory tract infections (6%), abdominal infections (6%), urinary tract infections (1%), and unknown (29%). The most common pathogens causing BSI were coagulase-negative staphylococci (23%, 33 episodes), Staphylococcus aureus (13.5%, 19 episodes), and Candida spp. (13.5%, 19 episodes), and Pseudomonas aeruginosa (11.4%, 16 episodes) (Table 1). Bloodstream infections with vancomycin-resistant enterococcemia occurred in 5 patients.


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  		Table 1. Pathogens Accounting for 140 Nosocomial Bloodstream Infections In 104 Patients With Left Ventricular Assist Devices

 
The incidence of BSI by LVAD device are shown in Table 2. The overall interval from implant of device to onset of BSI was 23 days. Although not statistically significant, there was a difference in the median interval from implant of device to onset of BSI by pathogen group (Fig 1). The median interval from implant to BSI was 28 days for fungi, 24 days for gram-positive cocci, and 19.5 days for gram-negative bacilli.


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  		Table 2. Incidence of Nosocomial Bloodstream Infections (BSI) by Device

 


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  		Fig 1. Interval from implantation of left ventricular assist device (LVAD) to onset of nosocomial bloodstream infection, by pathogen group.

 
There was no significant difference in the Kaplan-Meier estimates of infection-free time by type of LVAD device (p = 0.42) (Fig 2). There was no host factor significantly associated with an increased risk for nosocomial BSI (Table 3). There was no significant difference from admission to our hospital and subsequent implantation of LVAD for patients with and without nosocomial BSI (11.9 days for patients with BSI versus 11.6 for patients without BSI, p = 0.9).



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  		Fig 2. Kaplan-Meier (K-M) estimates of infection-free time (nosocomial bloodstream infections) by type of left ventricular assist device.

 

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  		Table 3. Potential Risk Factors for Nosocomial Bloodstream Infection (BSI) in Patients With Left Ventricular Assist Devices

 
We also assessed the impact of BSI on death on device (all patients) and survival to transplant. There were 60 patients who died with an LVAD, of which 5% (3 patients including 2 with nosocomial BSI) the cause of death was attributed to sepsis. Bloodstream infections were marginally significantly associated with increased mortality on device (58% versus 42%, p = 0.07) and decreased survival to heart transplantation among the 208 bridge to transplant patients (56% versus 44%, p = 0.08) (Table 4).


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  		Table 4. Impact of Nosocomial Bloodstream Infection (BSI) on Survival in Patients With Left Ventricular Devices

 
Two Cox proportional hazard models were run for time until death on device. The occurrence of an infection was treated as a time-dependent covariate. A model using only BSI identified it to be a highly significant factor associated with death on device (p < 0.001). A second model including device type found no significant association of device type with death on device, but BSI remained significantly associated with death on device (p < 0.001) (Table 5). When BSI were stratified by pathogen groups, fungemia had the highest hazard ratio (10.9) for death on device followed by gram-negative bacteremia (5.1) and gram-positive bacteremia (2.2).


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  		Table 5. Cox Models: Death on Device

 
Six-month survival for the 149 patients (72%) who underwent cardiac transplantation was not significantly affected by a nosocomial BSI after LVAD implantation (95% for patients without a BSI versus 87% for patients with BSI, p = 0.18) (Fig 3).



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  		Fig 3. Kaplan-Meier (K-M) estimates of 6-month survival for patients who underwent cardiac transplantation with and without prior nosocomial bloodstream infection on left ventricular assist device support.

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
The most important findings of our study are that patients with implantable ventricular assists devices have a high incidence of nosocomial BSI (approximately 8 per 1000 device-days), which are associated with increased mortality on device support. The associated increased mortality on device was highest for fungemia, followed by gram-negative bacteremia and gram-positive bacteremia. Infections associated with LVAD have significant implications but do not necessarily preclude successful transplantation. We found no significant difference between the incidence of nosocomial BSI in patients with LVAD when stratified by type of device implanted.

Infections have been a common complication reported in patients with implantable left ventricular assist devices [1, 6]. Multiple factors probably contribute the pathogenesis of infection in these patients, but first and foremost is that all of the currently available Food and Drug Administration-approved implantable LVAD have a transcutaneous line that carries the electrical cable and air vent to the battery pack and electronic controls. The 13.5- to 15-mm diameter drive line breaches the normal cutaneous barrier against infection and serves as a major portal of entry for pathogens. Recently published studies using pulsed field gel electrophoresis analysis of isolates obtained from the bloodstream and the drive line support the clinical observation that the drive line is a major portal of entry for nosocomial BSI in patients on LVAD support [7, 8]. Second, recipients of LVAD are critically ill by definition, often malnourished with multiple invasive supportive devices. Third, use of broad spectrum antimicrobial therapy is common, often empiric, prophylactic, or for treatment of infections in critically ill patients.

A review of published reports of infections in patients with implantable LVADs with an emphasis on BSI reveal results comparable to our findings (Table 6). The overall attack rates of infection in patients with LVADs was 34% (range, 4.5% [wounds only] to 51.4%) [7, 9–15]. The overall attack rate for BSI among patients with LVADs was 38% (162 episodes in 425 patients) (range, 16%–53%) [7, 9, 12, 16–18]. The overall incidence of BSI was 5 per 1000 device-days (range, 1.8 to 7.9) [9–12, 17, 18].


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  		Table 6. Infections in Patients With Left Ventricular Assist Devices (LVAD) With an Emphasis on Bloodstream Infections (BSI)

 
The most common bloodstream pathogens causing BSI in our patients were gram-positive cocci (coagulase-negative staphylococci and S aureus). Fungemias accounted for 16% of the 104 nosocomial BSI in patients on LVAD and was ominously associated with a 10-fold higher risk of death on LVAD support than patients without BSI. The onset of fungemia was later than other pathogens groups (Fig 2), probably reflecting in part prior antibacterial antibiotic exposure. The use of antibiotics may lead to development of infections with fungi and multiply resistant pathogens (eg, vancomycin-resistant enterococci). Candida spp, the most common fungal bloodstream pathogen in our patients, are increasingly identified as a cause of nosocomial BSI and associated hospital mortality. Skinner and colleagues [19] have recently reported on the burden of fungal infection or colonization in their patients with LVADs (44% of 36 patients). In this study, extended antifungal prophylaxis (use of azole or nystatin until all patients were extubated and all antibiotics were discontinued) was no more effective than use of antifungals for documented fungal colonization or infections.

There has been increased interest in the immunologic effects of LVAD implantation and associated infections with progressive defects in cellular immunity that may be the result of T-cell activation. These defects have been associated with increased risk of Candida and other systemic infections [20]. Targeted approaches to downregulate abnormal immune reactivation in LVAD recipients may reduce the infection risk in patients on long-term support.

There were several limitations to our study. The data were collected retrospectively and specific information on antibiotic days and drive line cultures were not abstracted. We also used an epidemiologic definition of LVAD-associated BSI, which may have underestimated the true number of device-associated BSI.

The management of LVAD-associated infections, including BSI, has been challenging. We have classified LVAD-associated infections along a clinical spectrum that includes prosthetic valve endocarditis (involvement of either of the porcine valves or grafts on the inflow or outflow tracts), pocket infections or drive line infections. Some low-grade infections of the drive line or tunnel have been treated successfully with local wound care and treatment with less than 14 days of antibiotics. Other patients have relapsed after stopping antimicrobial therapy and have required chronic suppressive antibiotic treatment until transplantation. Surgical management of the LVAD infections (revisions of the infected pump pocket, drive line tunnel, or device exchange) have also been attempted. In our experience, device replacement carries a higher perioperative mortality and risk of relapse and has been restricted to patients with intractable sepsis syndrome or multiple septic embolic in the setting of maximal medical therapy.

Strategies for prevention of infection in LVAD recipients should focus on the drive line exit site. At our institution ongoing efforts to reduce drive line infections include (1) placement of the transcutaneous exit site on the side of the abdomen contralateral to where the LVAD pump pocket is placed to have a longer subcutaneous course and barrier to infection, (2) postoperative care emphasizing early immobilization of the drive line to promote granulation tissue to occur, (3) use of a silver-impregnated dressing at the exit site (Arglaes film, Maersk Medical Ltd, Mundelein, IL) and plans for use of antimicrobial impregnated drive line [21], (4) judicious use of antimicrobial agents in the perioperative period with no routine continuous antimicrobial prophylaxis, and (5) studying the effect of antimicrobial drive line coating.

Future strategies for prevention of LVAD-associated BSI are directed at eliminating the portal of entry, the transcutaneous drive line. Engineering efforts have produced prototypes for continuous flow (nonpulsatile) LVADs, with smaller transcutaneous drive lines, and transcutaneous energy transmission [22].


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Goldstein D.J., Oz M.C., Rose E.A. Implantable left ventricular assist devices. N Engl J Med 1998;339:1522-1533.[Free Full Text]
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  3. McCarthy P.M., Schmitt S.K., Vargo R.L., Gordon S.M., Keys T.F., Hobbs R.E. Implantable LVAD infections. implications for permanent use of the device. Ann Thorac Surg 1996;61:359-365.[Abstract/Free Full Text]
  4. McCarthy P.M., Sabik J.F. Implantable circulatory support devices as a bridge to heart transplantation. Semin Thorac Surg 1994;6:174-180.
  5. Garner J.S., Jarvis W.R., Emori T.G., Horan T.C., Hughes J.M. CDC definitions for nosocomial infections. Am J Infect Control 1988;16:128-140.[Medline]
  6. Piccione W. Left ventricular assist device implantation: short and long-term surgical complications. J Heart Lung Transplant 2000;19:589-594.
  7. Herrmann M., Weyand M., Greshake B., et al. Left ventricular assist device infection is associated with increased mortality but is not a contraindication to transplantation. Circulation 1997;95:814-817.[Abstract/Free Full Text]
  8. Vilchez R, McEllistrem MC, Harrison LH, et al. Relapsing bacteremia in patients with ventricular assist device as a bridge for transplantation. 38th Annual Meeting of Infectious Disease Society of America, September 7–10, 2000, New Orleans, Abstract 143.
  9. Fischer S.A., Trenholme G.M., Costanzo M.R., Piccone W. Infectious complications in left ventricular device assist device recipients. Clin Infect Dis 1997;24:18-23.[Medline]
  10. Prendergast T.W., Todd B.A., Beyer A.J., et al. Management of left ventricular assist device infection with heart transplantation. Ann Thorac Surg 1997;64:142-147.[Abstract/Free Full Text]
  11. Malani PN, Dyke DB, Chenoweth CE. Nosocomial infections in left ventricular assist devices. 38th Annual meeting of Infectious Disease Society of America, September 7–10, 2000. New Orleans. Abstract.
  12. Springer W.E., Wasler A., Radovancevic B., et al. Retrospective analysis of infection in patients undergoing support with left ventricular assist systems. ASAIO Journal 1996;42:M763-M765.[Medline]
  13. Peterzen B., Granfeldt H., Lonn D., et al. Management of patients with end-stage heart disease treated with an implantable left ventricular assist device in a nontransplanting center. J Cardiothoracic Vasc Anesth 2000;14:438-443.[Medline]
  14. Tjan T.D.T., Asfour B., Hammel D., et al. Wound complications after left ventricular assist device implantation. Ann Thorac Surg 2000;70:538-541.[Abstract/Free Full Text]
  15. Griffith B.P., Kormos R.L., Mastala C.J., Winowich S., Pristas J.M. Results of extended bridge to transplantation: window into the future of permanent ventricular assist devices. Ann Thorac Surg 1996;61:396-398.[Abstract/Free Full Text]
  16. Argenziano M., Catanese K.A., Moazami N., et al. The influence of infection on survival and successful transplantation in patients with left ventricualr assist devices. J Heart Lung Trans 1997;16:822-831.[Medline]
  17. Arusoglu L., Koerfer R., Tenderich G., et al. A novel method to reduce device-related infections in patients supported with the HeartMate device. Ann Thorac Surg 1999;68:1875-1877.[Abstract/Free Full Text]
  18. Holman W.L., Skinner J.L., Waiter K.B., et al. Infection during circulatory support with ventricular assist devices. Ann Thorac Surg 1999;68:711-716.
  19. Skinner J.L., Harris C., Aaron M.F., et al. Cost-benefit analysis of extended antifungal prophylaxis in ventricular assist devices. ASAIO J 2000;45:587-589.
  20. Ankersmit H.S., Tugulea S., Spanier T., et al. Activation of T-cell death, and immune dysfunction after implantation of left ventricular after implantation of left ventricular device. Lancet 1999;354:550-555.[Medline]
  21. Choi L., Choudhri A.F., Pillarisetty V.G., et al. Development of an infection-resistant LVAD driveline: a novel approach to the prevention of device-related infections. J Heart Lung Transplant 1999;18:1103-1110.[Medline]
  22. Meyers T.J., Khan T., Frazier O.H. Infectious complications associated with ventricular assist systems. ASAIO J 2000;46:S28-S36.[Medline]



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