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Ann Thorac Surg 2001;72:96-101
© 2001 The Society of Thoracic Surgeons

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Original article: cardiovascular

Relapsing bacteremia in patients with ventricular assist device: an emergent complication of extended circulatory support

Accepted for publication April 3, 2001.

Address reprint requests to Dr Kusne, Division of Infectious Diseases, University of Pittsburgh Medical Center, 501 Kauffman Bldg, 3471 Fifth Ave, Pittsburgh, PA 15213
e-mail: kusnes2{at}msx.upmc.edu

	Abstract

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

 
Background. Ventricular assist devices (VAD) are currently approved for use as a bridge for transplantation. Although reports have suggested acceptable rates of survival of patients with VAD, there is little information regarding the mechanism and etiology of bacteremia in these patients.

Methods. We prospectively followed patients who underwent VAD implantation and developed bacteremia during VAD support at the University of Pittsburgh Medical Center. Relapsing bacteremia was defined as at least two episodes of positive blood cultures with a genetically related organism on 2 different days. Species identification and susceptibility testing were performed on all isolates. Pulse field gel electrophoresis was performed on selected blood and VAD isolates.

Results. Between January 1998 and August 1999, 3 patients with VAD developed relapsing bacteremia, which was treated with full courses of antibiotic agents, 2 of whom also developed VAD endocarditis. All 3 patients had documented driveline or device pocket infections with these isolates. Consecutive blood and VAD isolates were found to be genetically related within each patient.

Conclusions. These patients with bacteremia after VAD implantation had relapse due to the same strain, which may have originated from indolent driveline infection. Endovascular infection in this setting is difficult to eradicate with antibiotic agents and carries a high mortality. These patients should be considered to have priority for orthotopic heart transplantation.

	Introduction

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

 
An estimated 20,000 patients in the United States would benefit from heart transplantation, but only 2,300 transplant operations are performed annually because of limited donor supply [1]. During the last decade, mechanical circulatory support with ventricular assist devices (VAD) has revolutionized the care of patients with heart failure who are awaiting cardiac transplantation [2]. Several VAD have received Food and Drug Administration approval for use as a bridge for transplantation. These implanted pumps serve to unload the left ventricle and allow ambulation and improved end-organ perfusion before transplantation. Mechanical circulatory support devices usually provide pulsatile flow, are internal, and are either pneumatically or electrically driven [3].

As the number of patients with heart failure grows each year, the Institute of Medicine has estimated that by the year 2010, as many as 70,000 patients could benefit from these devices [1]. Furthermore, because the average waiting time for a donor heart has increased during the past few years, there has been an interest in expanding VAD use from short-term to long-term use, and perhaps for permanent support. Indeed, the presumed comfort with the use of these devices in a chronic mode has been incorporated into the decision making for the United Network of Organ Sharing (UNOS) status listing criteria. After 30 days of support patients on VAD are downgraded from status 1a to status 1b based on presumed stability. Only when and if the patient has a complication that warrants an admission, is the patient’s status raised [4].

Infections in patients during VAD support have been associated with substantial morbidity and mortality [5–10], and may have serious implications for long-term use. However, only minimal data are available concerning the clinical spectrum, mechanism, and management of VAD-related bloodstream infection, and the impact on subsequent transplantation. We present 3 patients with relapsing bacteremia during prolonged mechanical circulatory support with a VAD and discuss the mechanism, etiology, clinical significance, and implications for its extended use. Molecular subtyping must be performed to confirm that a recurrent bacteremia is from the same bacteria, that is, relapsing bacteremia. Pulse field gel electrophoresis (PFGE), a robust molecular subtyping method, can differentiate bacterial strains that appear identical by routine antimicrobial susceptibility test.

	Material and methods

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

 
Patients and definitions
The patients described in this report underwent insertion of the Novacor-LVAD or Thoratec-RVAD system at the University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania. The patients were approved cardiac transplant candidates and had New York Heart Association class IV despite the use of inotropic agents and conventional medical therapy. Extended VAD support was defined as more than 200 days of mechanical circulatory support. Relapsing bacteremia was defined as at least two episodes of positive blood cultures on 2 different days with genetically related organism. The bacteria were defined as genetically related if there were three or fewer bands’ difference in their PFGE [11]. Detailed medical records were kept prospectively for each patient and data collected included dates and type of device implantation, blood culture reports, antibiotic agents received, and outcome.

Laboratory methods
Blood cultures
Blood cultures were obtained by peripheral venipunctures. Ten milliliters of blood was obtained using standard antiseptic technique. Blood samples from each draw were inoculated in aerobic and anaerobic media and processed using the BacT/Alert Blood Culture System (Organon-Teknika Corporation, Durham, NC).

Pulse field gel electrophoresis
The bacterial DNA was extracted and cut with an enzyme as described below. Each DNA sample was then loaded into a corresponding lane of an agarose gel. The DNA fragments were separated by size with gel electrophoresis. Genomic DNA for Enterococcus faecium, Enterococcus faecalis, Staphylococcus coagulase negative, Pseudomonas aeruginosa, and Proteus mirabilis was prepared as described elsewhere [12–14]. Briefly, cultures were grown overnight on trypticase soy agar with 5% sheep blood (Baltimore Biological Laboratory) and suspended in 2 mL of TE buffer (10 mM Tris-HCl and 1 mM of EDTA; pH 7.6) to an optical density of 0.6 to 0.7 at 450 nm. The bacterial suspension was mixed with an equal amount of 2% low melting agarose (Sea Plaque, FMC Bioproducts, Rockland, ME) and pipetted into 100 µL plug molds. The E faecalis and E faecium plugs were lysed with 3 mL of lysis buffer (1 M NaCl, 100 mM EDTA, 6 mM Tris-HCl, 0.5% Brig-58, 0.5% deoxycholate, 0.5% N-lauroyl sarcosine, 1 mg/mL lysozyme; pH 7.6) overnight at 37°C. Next, each plug was incubated with 2 mL of ESP buffer (0.5 M EDTA, 1% N-lauronyl sarcosine, 1 mg/mL of proteinase K; pH 8.0 to 8.5) for 3 hours at 50°C. The plugs were then washed three times with 10 mL of TE buffer.

For P mirabilis, two methods were used to avoid DNA degradation. The first protocol was as described above except the lysis buffer also included 50 µg/mL ribonuclease A and the plugs were incubated in ESP overnight. The second protocol deleted the lysis buffer and lengthened the ESP incubation to 72 hours. For P aeruginosa, the procedure was as described above except the lysis buffer was omitted and the strains were incubated in ESP overnight. For S coagulase negative, the lysis buffer contained lysostaphin at 100 µg/mL (Ambi, Inc, Tarrytown, NY) instead of lysozyme and plugs were incubated at 55°C for 1 hour before TE buffer washes.

After DNA digestion with 50 U of enzyme and recommended restriction buffer (Boehringer Mannheim, Indianapolis, IN), PFGE was performed with CHEF DRIII. The enterococcal strains were electrophoresed at 1 to 30 seconds for 18.5 hours and 5 to 9 seconds for 8 hours after restriction with SmaI. The P aeruginosa strains were electrophoresed at the following run parameters for the two restriction enzymes: XbaI, 1 to 15 seconds for 4 hours then 5 to 10 seconds for 24 hours; SpeI, 5 to 25 seconds for 20 hours then 30 to 60 seconds for 4 hours. The P mirabilis strains were electrophoresed at both 5 to 45 seconds and 5 to 90 seconds for 20 hours after restriction with SfiI. For Staphylococcus epidermidis, the pulse time was 5 to 40 seconds for 20 hours after restriction with SmaI. After staining in ethidium bromide, the gels were captured on the Bio-Rad Gel Doc 2000 System (Bio-Rad, Hercules, CA).

	Case reports

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

 
Patient 1
A 50-year-old white man with ischemic cardiomyopathy received a Novacor-LVAD system on March 26, 1998. His immediate postoperative course was complicated by mediastinal hematoma, which was evacuated. At day 29 postimplant he developed acute right ventricular failure and received a Thoratec-RVAD. The patient did well until day 59 postimplant when he developed fever (38.6°C) and drainage at the Novacor-LVAD driveline site. Blood and driveline cultures were positive for oxacillin sensitive Staphylococcus aureus. He was treated with intravenous nafcillin and oral rifampin for 6 weeks. The patient improved and stabilized. At day 102 postimplant he developed increased drainage from Thoratec and Novacor driveline sites. Cultures from these places were positive for P mirabilis and S aureus, blood cultures remained negative. The patient’s drivelines were treated with local irrigations of vancomycin and gentamicin twice a day. However, the Novacor-LVAD driveline site culture was still positive for S aureus, so he was given intravenous vancomycin for 6 weeks. Between August and December 1999, he received a few more courses of intravenous antibiotics for increased drainage at the driveline sites. At day 307 postimplant, he developed fever (38.8°C) and chills. Blood cultures were positive for P mirabilis and S coagulase negative. The Thoratec-RVAD driveline culture was positive for P mirabilis. The patient was treated with intravenous vancomycin and gentamicin. He improved and subsequent blood cultures were negative. At day 370 postimplant, drainage was again observed from the Novacor-LVAD and Thoratec-RVAD driveline sites. Cultures from each driveline site were positive for P mirabilis. He was treated by irrigation of the driveline sites with gentamicin three times a day. Eleven days later, the patient developed fever (38.8°C) and the blood culture obtained was positive for S coagulase negative. The patient was started on intravenous vancomycin, but fever persisted and repeated blood cultures were positive for P mirabilis. He was then started on intravenous ofloxacin for 6 weeks. The patient improved and did well until day 417 postimplant when he developed fever (38.6°C) and his blood culture was positive for P mirabilis and E faecium (VRE). He was initially treated with intravenous ofloxacin. Repeated blood culture 3 days later was positive for E faecium (VRE) and E faecalis. The patient was then started on intravenous synercid and doxycycline. However, 1 week later he developed severe myalgias, so synercid was discontinued and was substituted with intravenous chloramphenicol. The repeated blood cultures during and after completion of therapy were negative. He did well until day 450 postimplant when he suddenly became hypotensive and was transferred to the intensive care unit. His blood cultures were reported positive for E faecium, E faecalis, and P mirabilis. The Thoratec-RVAD and Novacor-LVAD driveline sites cultures were positive for P mirabilis, E faecalis, and Candida albicans. He was treated with intravenous imipenen, tobramycin, synercid, and ampicillin. The patient improved and the repeated blood culture 5 days later was negative. At day 467 postimplant, he developed a large hemorrhagic stroke in the left parietal lobe with extension into lateral and third ventricules. The patient died 2 days later. At autopsy, cultures from the Novacor-LVAD inflow and outflow valves and the implantation site were positive for E faecium. The Thoratec-RVAD outflow valve was positive for E faecalis and S coagulase negative.

Patient 2
A 51-year-old white man with idiopathic dilated cardiomyopathy underwent a Novacor-LVAD implantation on March 26, 1998. His postoperative course was uncomplicated and he was discharge three weeks later. At day 55 postimplant, he was readmitted with complaints of fever (39°C) and chills. Culture from the driveline site yielded P aeruginosa, but the blood culture was negative. The patient was treated with intravenous ceftazidime and oral ofloxacin for 14 days. At day 131 postimplant he was admitted with fever (38.8°C), myalgias, and aching around the Novacor-LVAD driveline site. Driveline site culture was again positive for P aeruginosa, but blood culture was negative. He was treated with intravenous tobramycin, and piperacillin. He continued to have a purulent drainage from LVAD driveline and 13 days after his admission, he underwent surgical debridement of Novacor-LVAD driveline site. He received 2 more weeks of intravenous antibiotics and was discharged on oral ciprofloxacin for 4 more weeks.

On day 172 postimplant, he was readmitted complaining of fever (39°C) and malaise. This time his driveline site and blood cultures were both positive for P aeruginosa. The patient was started on intravenous tobramycin and imipenen. He was discharged home to complete a 6-week course of intravenous antibiotic agents. At day 212 postimplant, he was readmitted with fever (40°C) and purulent drainage from the LVAD driveline site. A culture from the Novacor-LVAD driveline site was positive for P aeruginosa, but his blood culture remained negative. The patient was treated with intravenous tobramycin and imipenen. He did well until day 227 postimplant when he again developed fever (38.6°C). The blood culture was positive for P aeruginosa. The patient was continued on intravenous tobramycin and imipenen. Blood culture repeated 7 days later was negative. On November 19, 1998, his Novacor-LVAD system was found to be nonfunctional and he underwent replacement of his device. Cultures from inflow and outflow valves of the removed device grew P aeruginosa. He was continued on intravenous antibiotics for 6 more weeks and also irrigation of the new Novacor-LVAD driveline site with tobramycin three times a day.

At day 299 post-implant, he developed fever (38.8°C). Blood and LVAD driveline cultures were positive for P aeruginosa. The patient was started on intravenous cefepime and tobramycin. Despite continued intravenous antibiotic agents, repeated blood cultures over a few weeks were still positive for P aeruginosa. At day 374 postimplant a heart donor was found and the patient underwent successful orthotopic heart transplantation. Cultures from the Novacor-LVAD inflow and outflow valves and the implantation site were positive for P aeruginosa. Subsequent blood cultures were negative, after removal of the device and heart transplantation. The patient continues to do well 2 years after his transplant operation.

Patient 3
A 41-year-old black man with idiopathic dilated cardiomyopathy underwent implantation of a Novacor-LVAD on September 10, 1998. Nineteen days after device implantation the patient underwent surgical evacuation of a large hematoma secondary to bleeding at the implant site. He was discharged home 16 days later. At day 54 postimplant, the patient noticed increased drainage from the Novacor-LVAD driveline site. A culture from the driveline site yielded oxacillin-sensitive Staphylococcus aureus. The patient was started on intravenous nafcillin and oral rifampin. He did well until day 165 postimplant, when he developed increased driveline site drainage, which grew P aeruginosa. The patient was treated by local irrigation of the driveline site with tobramycin two times a day for 2 weeks. At day 206 postimplant, he was admitted to the hospital complaining of pressure next to the driveline site but without fever or chills. Driveline site and blood cultures were positive for P aeruginosa. A computed tomography scan of the abdomen showed a fluid collection adjacent to the LVAD. The collection was drained, and the patient was treated with intravenous tobramycin and cefepime for 3 weeks, followed by oral ciprofloxacin for 2 more weeks. At day 283 postimplant the patient was readmitted with temperature elevation and increased driveline site drainage. Cultures from the LVAD driveline site and blood were again positive for P aeruginosa. He was started on intravenous cefepime and tobramycin. Subsequent blood cultures were negative. At day 307 postimplant the patient underwent orthotopic heart transplantation. He developed primary allograft failure and died 1 day later. Cultures from the LVAD and explantation site were positive for P aeruginosa.

	Results

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

 
Table 1 summarizes the total number of days of VAD support, positive blood cultures, identified blood organism, and VAD isolates from each patient. The PFGE patterns of P mirabilis (n = 8) and coagulase negative Staphylococcus (n = 7) isolated during the course of VAD support from patient 1 blood cultures were indistinguishable. Also patient 1’s initial E faecium blood isolate was genetically related to the E faecium isolates from the VAD inflow and outflow valves.

View larger version (147K): [in this window] [in a new window]   Fig 1. Pulse field gel electrophoresis patterns of Pseudomonas aeruginosa isolates. Each vertical lane (lanes 2–17) contains one bacterial isolate of P aeruginosa. Lane 1 is the lambda ladder control marker. Lanes 2–4 represent P aeruginosa control strains, that is, isolates from patients that do not have a ventricular assist device. Lanes 5–12 represent the eight P aeruginosa isolates from patient 2. Lanes 13–17 represent the five P aeruginosa isolates from patient 3.

	Comment

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

In a study of 20 patients with VAD, Fisher and colleagues [6] described three cases of bacteremia with S aureus and coagulase negative Staphylococcus. However, the length of VAD support was relatively short (range 35 to 115 days) and no relapse was observed. In a second report of 33 VAD recipients, 12 developed episodes of bacteremia during mechanical circulatory support [10]. The organisms involved included Staphylococcus sp, Candida sp, P aeruginosa, and E faecalis. The mean duration of VAD support was 72 ± 34 days (range 22 to 153 days). No relapse occurred after antibiotic therapy and the patients underwent successful heart transplantation.

Compared with these reports, our patients received extended periods of VAD support, which substantiates previous reports suggesting that the incidence of infection is proportional to the duration of mechanical circulatory support [16, 17]. In a review of 162 patients who received VAD support, the incidence of infectious complication in patients who had 60 to 100 days of mechanical circulatory support was lower than those who had support for more than 100 days (37% versus 55%) [16]. Recent studies have indicated that after VAD implantation, patients have diminished reactivity to recall antigens. Patients with VAD have been found to have less than 70% T-cell proliferative response after activation by the T-cell receptor complex compared with a control group. T cells from VAD recipients had a higher surface expression of CD95 (Fas) (p < 0.001) and a higher rate of spontaneous apoptosis than controls (p < 0.001). Immunologic abnormalities may also play a role in the development of systemic infection in patients with VAD [18, 19].

Our study demonstrates an emerging spectrum of serious infections in patients with extended VAD support. The episodes of repeated bacteremias in these 3 patients despite prolong antibiotic therapy are suggestive of persistent endovascular infection resembling endocarditis. In support of this hypothesis, the cultures from the VAD inflow and outflow valves in 2 of the 3 patients at the time of device explantation were positive for the same organisms previously isolated from the blood. The results of PFGE of blood isolates with indistinguishable banding patterns indicates that recurrent bacteremia in these patients was a result of relapse from the same strain. Furthermore, the blood isolates and VAD valve isolates in 2 patients were identical, suggesting the device itself as the source of bacteremia.

To the best of our knowledge, only one previous report has described endocarditis in VAD recipients during extended circulatory support [5]. Eight of 29 patients with VAD were defined to have endocarditis by manifestations of systemic infection accompanied by positive culture from the removed device. However, only 3 of these 8 patients were reported to develop bacteremia. The average length of VAD support at the time of diagnosis was 112 ± 77 days. The possible sources of infection were identified in 7 patients and consisted of three driveline infections, one VAD pocket infection, two central venous catheter infections, and one sternal wound infection. Four patients died and only 2 of those who survived were reported to undergo heart transplantation. Similarly, only 1 of our patients was able to have successful heart transplantation.

In contrast to previous reports that VAD driveline infections are not associated with systemic complications [2], our investigation suggests that the relapsing bacteremia may have arisen from VAD drivelines. The possible contribution of VAD driveline infections to the development of relapsing bacteremia and VAD endocarditis in the course of extended circulatory support cannot be underestimated. Therefore, although these patients may be managed as outpatients, the seriousness of this complication and its long-term outcome may warrant reconsideration of how stable these patients really are on chronic support. The infections also bring into question the logic of not listing these patients as UNOS status 1a because ultimately infection makes transplantation more morbid. In addition, the recent development of VAD drivelines impregnated with antimicrobial agents may prevent early infections and facilitate ingrowth of tissue to provide long-term stability and protection against late infections [20].

In summary, our cases illustrated the complexity of an emerging pattern of endovascular infection in patients with extended VAD support. Indolent driveline infections may be the source of relapsing bacteremia and VAD endocarditis. Both conditions are difficult to eradicate with antibiotic agents and cause high mortality, suggesting that these patients should be considered to have a high priority for heart transplantation. Further studies are needed to define the risk and optimal therapy for these serious infections.

	Acknowledgments

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

 
We thank A. William Pasculle, ScD, for providing the clinical isolates, Carla Baxter for expert technical assistance, and Marlene Czarnecki, MS, for performing the pulse field gel electrophoresis on the study isolates.

	Footnotes

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

 
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/section/atsdiscussion/

	References

Top Footnotes Abstract Introduction Material and methods Case reports Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Kenneth R. McCurry Robert L. Kormos Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Vilchez, R. A. Articles by Kusne, S. Search for Related Content PubMed PubMed Citation Articles by Vilchez, R. A. Articles by Kusne, S. Related Collections Mechanical Circulatory Assistance