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Ann Thorac Surg 1996;61:359-365
© 1996 The Society of Thoracic Surgeons
Departments of Thoracic and Cardiovascular Surgery, Infectious Disease, and Cardiology, The Cleveland Clinic Foundation, Cleveland, Ohio
Abstract
Background. Infection in implantable left ventricular assist device (LVAD) patients is common and has serious implications regarding permanent use of the LVAD.
Methods. Thirty-three patients had HeartMate LVAD insertion as a bridge to heart transplantation. The mean length of hospital stay was 8 days before LVAD insertion. Before insertion 6 patients (18%) had positive pulmonary cultures and 5 patients (15%) had bacteremia.
Results. During LVAD support 18 patients (55%) had bloodstream infection. Of 24 patients (73%) successfully bridged to transplantation, 12 (50%) had positive blood cultures including Staphylococcus species (n = 9), Candida (n = 3), Pseudomonas (n = 2), and Enterococcus (n = 2). Infectious complications encountered in this series included driveline infection requiring surgical revision, septic embolus, ``cleared'' device infection, ``suppressed'' device infection, and LVAD infection treated by device removal in 1 patient and device exchange in another.
Conclusions. Infection in implantable LVAD patients is common, especially in patients in whom multiple organ failure develops, requiring prolonged stay in the intensive care unit. Strategies are needed to prevent these infections in recipients of the permanent LVADs because treatment of an established infection is difficult and expensive.
New technology used in the implantable left ventricular assist device (LVAD) has successfully addressed previous clinical problems with mechanical circulatory support systems. These advances include the use of portable battery powered systems, which allow the patient more mobility [1–3], a low risk of thromboembolic events [3–5], preliminary studies that indicate a quality of life similar to that of patients after heart transplantation [6], and outpatient use of the implantable LVAD [7]. Hemodynamic and physiologic improvement in the LVAD recipient have been impressive [8–11]. However, device infection has been an important source of morbidity [8, 9, 12–14] and has serious implications for the anticipated application of LVADs as permanent therapy. Infection of the permanently implanted device could lead to rehospitalization, septic emboli, and reoperations including revisions of the percutaneous driveline, and removal or exchange of the infected device. These morbidities would have a significant negative impact on quality of life and lead to increased cost of LVAD treatment. Eventually device-related infection could become a major risk for mortality in patients receiving the implantable LVAD as permanent therapy.
This report reviews the Cleveland Clinic experience with the HeartMate implantable LVAD (Thermo Cardiosystems, Inc, Woburn, MA) when used as a bridge to heart transplantation. Representative case studies are presented of patients with infection while on LVAD support, and our surgical and medical treatments for this dreaded complication.
Material and Methods
The HeartMate LVAD is a pusher-plate implantable device with a titanium pump housing [3, 4]. Inflow to the pump through the left ventricular apex is through a porcine-valved conduit that lies underneath the left costal margin. Outflow from the pump is via a valved conduit and graft, which return to the ascending aorta and lie just to the right of the midline underneath the sternum [14].
There are currently two HeartMate systems. The first system is the HeartMate 1000 IP air-driven system, which is Food and Drug Administration (FDA) approved as a bridge to cardiac transplantation. It weighs 0.7 kg. The percutaneous pneumatic driveline is approximately 1 cm across and covered in Dacron. In our patients the driveline exits the skin in the left lower abdominal quadrant, and 8 cm of Dacron-covered driveline are typically within the patient's subcutaneous tissue. The second system is a portable, vented, electrically powered device. It also has a percutaneous Dacron-covered vent line exiting the left lower quadrant (as of December 1994), and a smaller Dacron-covered electrical power line that exits through the right mid-abdominal wall. Therefore, the pneumatic 1000 IP HeartMate has a single percutaneous vent line, and the vented-electric system currently has two percutaneous lines. Plans are underway to modify the vented-electric HeartMate LVAD so that there is a single percutaneous line containing both the power source and vent. This new system is being reviewed for FDA approval. The vented-electric HeartMate is still experimental and under FDA investigational device exemption use. The vented-electric LVAD weighs 0.9 kg, also is housed in titanium, and has the same valved conduits and textured blood-contacting surfaces as the 1000 IP.
The HeartMate LVAD had typically been placed within the abdominal cavity by most investigators [4, 13], and this technique was used in our first HeartMate patient at The Cleveland Clinic. However, this places the pump immediately adjacent to the liver, colon, omentum, and stomach with the potential for visceral erosion, bowel obstruction, and diaphragmatic hernia [4, 13]. Therefore, we implanted the pump in a preperitoneal pocket on top of the posterior rectus sheath and below the rectus muscle [3, 14]. Therefore the device was no longer in direct contact with abdominal viscera but was in a surgically created pocket in the abdominal wall.
The patients described in this report received the HeartMate LVAD as part of an experimental study before FDA approval of the HeartMate 1000 IP. The inclusion and exclusion criteria of the FDA study have been previously reported [4]. Briefly, all patients were approved cardiac transplant candidates who were in cardiogenic shock despite the use of inotropes and conventional medical therapy.
Patients were not excluded if they had an infection that was thought to be treatable. The only exception was a patient who was thought to have resolving pneumonia before LVAD operation and was found at the operation to have purulent pericarditis. Because of the inevitability of device infection in this setting, the patient was closed without insertion of a HeartMate device and was treated with high-dose antibiotics. He died secondary to low cardiac output and ventricular arrhythmias 36 hours after operation. Blood cultures later grew Candida albicans.
Thirty-three patients underwent HeartMate LVAD insertion by one surgeon from December 1991 until October 1994. This group included 29 patients who received the HeartMate 1000 IP pneumatic device and 4 patients who received the vented-electric HeartMate LVAD at their initial operations. The mean age of the patients was 51 years, and the group included 28 male patients (85%). The underlying cardiac diagnosis was dilated cardiomyopathy in 10 (30%) and ischemic cardiomyopathy in 23 patients (70%).
All patients were in cardiogenic shock. In addition to inotropic support, 29 patients (88%) were also on an intraaortic balloon pump and 24 patients (73%) were also intubated because of pulmonary edema. Eight patients (24%) were in such profound cardiogenic shock that they could not be supported with just inotropes and intraaortic balloon pump alone, and were placed on heparin-coated extracorporeal membrane oxygenation to stabilize them and allow for heart transplantation evaluation and clearance before HeartMate LVAD insertion. The mean length of Cleveland Clinic hospital stay before HeartMate LVAD insertion was 8 days (range, 1 to 47 days), and the mean length of intensive care unit length of stay before HeartMate insertion was 5 days (range, 1 to 23 days).
After HeartMate insertion the percutaneous driveline insertion sites were treated with dressing changes three times per day using silver sulfadiazine cream in the initial 28 patients (as per the original HeartMate Investigator Training Program). The most recent 5 patients, however, have had dressing changes three times per day along with povidone-iodine solution treatment. A variety of antibiotic therapies were employed for this patient group according to the patients' preoperative cultures, renal function, overall condition, and likelihood for early extubation and rehabilitation. Patients who were moribund and not expected to be extubated early were generally treated with vancomycin and ceftazidime (53%). Forty-seven percent received perioperative cefuroxime. All patients also received nystatin orally twice per day until extubation.
Results
The mean cardiac index rose from 1.6 ± 0.3 to 2.9 ± 0.6 L•min-1•m-2 during the period of LVAD support. All patients who left the intensive care unit survived and received a transplant (n = 24; 73%); mean duration of support was 72 ± 34 days (range, 22 to 153 days). Nine patients (27%) never left the intensive care unit after LVAD insertion and died.
Six patients (18%) had bacterial or fungal growth from respiratory cultures and 5 patients had bloodstream infections during their pre-LVAD hospital course. There were a total of 23 episodes of bloodstream infection among 18 patients (55%) during LVAD support. Pathogens isolated from the bloodstream during LVAD support (Fig 1
) included Candida species (n = 7 patients; mean onset after LVAD implantation, 30 days), Staphylococcus aureus (n = 7; 17 days), Staphylococcus epidermidis (n = 4; 15 days), Enterococcus species (n = 3; 25 days), Pseudomonas aeruginosa (n = 2; 45 days), and Enterobacter species (n = 1; 4 days). Two episodes of bloodstream infection were polymicrobial: one with Enterococcus species and S aureus, and the other with Enterobacter species and S epidermis.
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. A Pseudomonas infection was detected on day 1 and most likely represented an infection acquired before LVAD insertion. Staphylococcus infections were most common from 2 to 3 weeks after LVAD insertion. Opportunistic infections (Candida and Pseudomonas) were more common later in the clinical course. The patients were divided in two groups: group A, the patients who were rehabilitated and successfully underwent transplantation (n = 24), and group B, patients who stayed in the intensive care unit until they died (n = 9). Group A patients more accurately reflect the patients who we think will have implications for permanent use of the device.
Group A
In group A, positive blood cultures developed in 12 patients (50%) while on LVAD support. The organisms identified included Staphylococcus species (n = 9), Candida (n = 3), Pseudomonas (n = 2), and Enterococcus (n = 2). All patients were given antibiotics or antifungal agents as appropriate. All devices were cultured at the time of explanation/heart transplantation. Of the 12 patients with bloodstream infection, cultures of the explanted device were positive in 9 patients (75%) despite the use of antibiotics. In 2 of 12 patients (17%) who had no clinical evidence of device infection or bacteremia, the device explant cultures were positive. In total, of 24 LVAD devices explanted, there were 11 positive cultures (46%). Because of presumed device or driveline infection 54% of patients (n = 13) were receiving suppressive antibiotics at the time of transplantation.
Group A patients were found to have positive driveline cultures from the skin insertion site in 50% (n = 12). One patient had what was thought to be a clinically significant percutaneous driveline infection and underwent surgical revision of the driveline and povidone-iodine irrigation of the pump pocket (patient 1). In other patients (n = 11) transient positive driveline cultures developed, frequently with low-grade fever, erythema, and tenderness, but these patients did not require surgical treatment and improved with intravenous antibiotics. Organisms identified included Staphylococcus species (n = 8), Enterococcus (n = 2), Diphtheroids (n = 2), Candida (n = 1), and Pseudomonas species (n = 1).
Driveline healing was variable. In most patients (Fig 2A) the driveline was firmly sealed with subcutaneous tissue incorporated into the Dacron fiber with a barrier to bacterial penetration into the pump or pocket. At device explantation these drivelines had to be surgically excised because of the strong bond to surrounding tissues. In other patients (Fig 2B) there was poor tissue ingrowth into the Dacron driveline.
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PATIENT 1.
The patient was a 55-year-old man transferred to us after emergency coronary bypass elsewhere. He underwent HeartMate 1000 IP insertion on September 19, 1992. He had a previous history of diabetes and obesity. He was transferred out of the intensive care unit on postoperative day 3. On day 13 the patient was noted to have purulent discharge from the driveline site and a small area of skin necrosis on the inferior portion of the driveline exit site. At that time, driveline cultures were positive for coagulase-negative S aureus. He had received a 4-day course of vancomycin for a fever while in the intensive care unit; he was receiving no antibiotics at the onset of the driveline infection. He was treated with vancomycin for 12 days with initial improvement of his symptoms. On post-LVAD day 32, serosanguinous drainage from the driveline site again developed; on day 37 fever developed to 39°C accompanied by rigors.
Blood cultures were positive for methicillin-sensitive S aureus and driveline cultures were positive for S aureus, Enterococcus, and rare Candida albicans. He was treated with vancomycin, ceftazidime, and fluconazole. There was little improvement. On day 65 the patient was taken to the operating room where the infected driveline insertion site (see Fig 2b) was excised and a new exit site was fashioned approximately 10 cm below the old site [14] (Fig 3). In addition, the lower aspect of the midline incision was reopened and the pump pocket was opened and evacuated of old clotted blood. It was copiously irrigated with saline and povidone-iodine solution. Drains were left in place and the patient received povidone-iodine irrigation through the drains for 5 days. Surgical cultures were positive for S aureus, Enterococcus, and rare C albicans. He continued treatment with antibiotics until cardiac transplantation after 76 days of support and 11 days after driveline revision. He became febrile hours before the transplant operation. Device cultures were positive for S aureus. He was treated with vancomycin for 4 weeks after transplantation. The patient underwent superficial debridement of the abdominal wound 13 days after transplantation and was discharged the next day. He has had no mediastinitis, pocket infection, or other serious infectious complications since cardiac transplantation.
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The patient made steady progress and was rehabilitated and underwent cardiac transplantation after 101 days of support. Cultures at device explantation were positive for C albicans (inflow, outflow, pump pocket), and small vegetations were noted inside the outflow graft (Fig 4). She was treated with amphotericin, vancomycin, and ceftazidime. On the 8th posttransplantation day, the patient complained of diplopia and visual field deficit. Computed tomographic scan showed an embolic event to the cerebellum, which was thought to have occurred intraoperatively. It was thought that this most likely was a septic embolus from the small vegetations within the pump outflow graft, which was manipulated during device explantation. However, another source of emboli could not be excluded. Her posttransplantation course was otherwise unremarkable except for a low-grade staphylococcal infection of the pump pocket, which required open debridement and reclosure on the 36th day after transplantation. The patient has not had any recurrence of Candida infection and continues with normal renal function.
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PATIENT 4.
The patient was a 37-year-old man who was transferred with end-stage cardiac failure including severe renal and hepatic dysfunction. He underwent HeartMate LVAD insertion on September 1, 1993. The patient made slow progress after LVAD insertion and was transferred out of the intensive care unit on postoperative day 30. The patient had required a tracheostomy for respiratory failure. On day 66 fever developed and blood cultures were positive for C albicans. The patient was treated with intravenous amphotericin B and oral fluconazole was added. Initially the patient improved with a decrease in fever, and pump flows (which were high during the period of active infection) returned to normal. Recurrent fever and Candida-positive blood cultures developed after amphotericin B administration was stopped. A low dose of amphotericin B was given and continued throughout the duration of support until the patient received a transplant after 153 days. At explantation the device grew Candida and the pump pocket culture was negative. There were no vegetations identified within the device. After transplantation the patient has had no further evidence of Candida and is well.
Group B
In group B, 2 patients died early (day 0, day 3) and 7 patients had a progressively downhill course after LVAD insertion despite adequate pump flows. Four of these 9 patients required insertion of a right ventricular assist device using a centrifugal pump in the early postoperative period, and 1 other patient had persistent right heart failure requiring inotropic support during 70 days of LVAD support. In these complex patients with multiple organ failure it was difficult to determine whether positive blood cultures were from central venous lines or from the HeartMate device. There were no driveline infections in these patients. Six patients had positive blood cultures including Candida (n = 5); Staphylococcus (n = 2), Enterobacter (n = 1), and Enterococcus species (n = 1). Patients died after a mean of 29 ± 27 days (range, 0 days to 70 days). Infection was thought to be the contributing cause of death in 2 patients, both of whom had development of infection after being severely disabled with multiple organ failure including renal failure, hepatic dysfunction, and pulmonary dysfunction. One patient illustrates our attempt at clearing the infection by device explantation and reinsertion.
PATIENT 5.
The patient was a 35-year-old man who was transferred to us in severe cardiogenic shock with renal, hepatic, pulmonary, and cardiac failure. He underwent HeartMate LVAD insertion on April 27, 1993. Initial pump flows maintained the cardiac index just greater than 2.2 L•min-1•m-2 with high-dose inotropes. Progressive multiple organ failure developed including renal and hepatic dysfunction. Over a period of weeks the inotropic support was weaned, but the patient had to be maintained on at least 5 µg•kg-1•min-1 of dobutamine or the pump index would drop to less than 2 L • min-1•m-2, and the central venous pressure would exceed 20 mm Hg. The pump index on support averaged 2.5 L•min-1•m-2. Positive sputum and urine cultures for Candida developed. A massive exsanguinating upper gastrointestinal bleed developed on day 32. The patient was emergently taken for oversewing of a bleeding gastric ulcer. Ascitic fluid from that operation grew Candida. The pump (which had been separated from the peritoneal cavity by the posterior rectus sheath and peritoneal layer) was bathed in abdominal and gastric content during this difficult operation. The patient then had multiple positive blood cultures for Candida despite the use of amphotericin B, fluconazole, and 5-flucytosine. Device removal was considered but the patient still had right heart failure and did not have any evidence of LV recovery and therefore it was not thought that he would survive LVAD removal [15, 16]. Therefore, replacement was performed on day 44: the LVAD was removed, including all inflow and outflow conduits, grafts, driveline, and suture material. All portions of the pump material were culture positive for Candida. After thorough irrigation of the mediastinum and pump pocket, a new LVAD was inserted and tunneled through a different driveline exit site. The new LVAD was not placed in the abdomen because of the previous gastric operation. All blood cultures were negative after this operation for 3 weeks. The patient began to improve and urine output returned temporarily. However, recurrent positive Candida blood cultures and worsening hepatic dysfunction developed. The patient was allowed to die after 70 days of support. Autopsy confirmed extensive multiple organ failure with Candida infection of the second pump.
Comment
Our review demonstrates a high rate of infection in this seriously ill patient population. We chose 5 case summaries that we thought had implications regarding permanent LVAD applications: patient 1 had a serious percutaneous driveline infection; patient 2, septic embolus; patient 3, bacteremia with device infection ``cleared'' with antibiotics; patient 4, Candida device infection ``suppressed'' until transplantation; and patient 5, Candida device infection treated by device exchange. We would expect that all of these infection scenarios (and many others) can be anticipated with permanent LVAD applications. Although 4 of the 5 cases reported eventually had a successful outcome this was primarily because the LVAD use was temporary. For permanent LVAD use the strategies (such as ``moving'' the infected driveline in patient 1, and suppressing the infection until transplantation) would not have been successful definitive treatment.
For permanent LVAD use different strategies will need to be developed. First, the patient population should be different. All of the patients in this report were end-stage with impending multiple organ failure. Hopefully for permanent implantations we will intervene sooner in the patients' course and avoid prolonged intensive care unit stay (and attendant infection risk) from comorbidity such as renal, hepatic, and pulmonary failure. The initial target population for permanent LVAD implantation most likely will not be as moribund as our current bridge to transplantation patients [17].
Second, the percutaneous systems [1, 2] allow us to use this technology sooner than waiting for totally implanted systems but carry risk from localized and ascending driveline infections. Theoretically this risk may be decreased by a long tunnel from the device in the preperitoneal pocket to the driveline exit site. Better materials to promote healing, perhaps with antibiotic impregnation, may also help. However, a completely sealed system, without percutaneous wires or vents, using transcutaneous energy transmission systems should continue to be the ultimate goal of this technology [8].
In this early clinical experience it is sometimes difficult to clearly determine a ``device infection.'' In particular it may be difficult to determine whether a bloodstream infection is derived from central venous catheters or from an infected LVAD. We have developed a preliminary classification of implantable LVAD infections that may help to standardize reporting of these infections:
15,000/µL In our experience with LVAD infections, there is no clear successful course of action. In 1 group B patient, multiple organ failure and Candida mediastinitis precluded subsequent transplantation, so the LVAD was removed. Although the patient survived the operation, he died secondary to low output within 24 hours. In another patient (patient 5) with persistent right heart dysfunction requiring inotropes, we replaced the LVAD. The device was reinserted into the preperitoneal pocket because the patient's abdomen had been opened for an extensive gastric operation. After temporary success the recurrent positive fungal blood cultures developed and the patient died. One patient (personal communication; Eric Rose, New York, NY) was managed successfully by LVAD replacement with subsequent survival until transplantation. Our 2 patients differed from the Columbia patient in that our patients had multiple organ failure, whereas the Columbia patient was otherwise stable and well. The group at Fairfax Hospital was able to irrigate the LVAD and mediastinum with continuous povidone-iodine solution before successful transplantation [13]. At Stanford a Candida-infected LVAD patient was also successfully bridged [8].
For some patients receiving permanent implants, device infection will become a serious source of morbidity. The ideal approach for patients who have shown some recovery of underlying left ventricular function would be a temporary period of device removal while the infection is aggressively treated [15, 16]. The patient could then undergo repeat LVAD insertion after the infection has cleared. Alternatively, if there has been no underlying cardiac recovery, then device explantation with reinsertion (ideally within the abdominal cavity if there was a previous preperitoneal insertion) may be the most successful strategy.
Footnotes
Presented at The Third International Conference on Circulatory Support Devices for Severe Cardiac Failure, Pittsburgh, PA, Oct 28-30, 1994.
Address reprint requests to Dr McCarthy, Department of Thoracic and Cardiovascular Surgery F-25, The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195.
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L. Arusoglu, R. Koerfer, G. Tenderich, W. A. Alexander, and A. El-Banayosy A novel method to reduce device-related infections in patients supported with the HeartMate device Ann. Thorac. Surg., November 1, 1999; 68(5): 1875 - 1877. [Abstract] [Full Text] [PDF]
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T. Mussivand, P. J. Hendry, R. G. Masters, M. King, K. S. Holmes, and W. J. Keon Progress with the HeartSaver ventricular assist device Ann. Thorac. Surg., August 1, 1999; 68(2): 785 - 789. [Abstract] [Full Text] [PDF]
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S. H. McKellar, B. D. Allred, J. D. Marks, C. G. Cowley, D. C. Classen, S. C. Gardner, and J. W. Long Treatment of infected left ventricular assist device using antibiotic-impregnated beads Ann. Thorac. Surg., February 1, 1999; 67(2): 554 - 555. [Abstract] [Full Text] [PDF]
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S. A. Hunt and O.H. Frazier Mechanical Circulatory Support and Cardiac Transplantation Circulation, May 26, 1998; 97(20): 2079 - 2090. [Full Text] [PDF]
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R. Jarvik, S. Westaby, T. Katsumata, D. Pigott, and R. D. Evans LVAD Power Delivery: A Percutaneous Approach to Avoid Infection Ann. Thorac. Surg., February 1, 1998; 65(2): 470 - 473. [Abstract] [Full Text] [PDF]
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S. M. Gordon, J. M. Serkey RN, T. F. Keys, T. Ryan, C. A. Fatica RN, S. K. Schmitt, J. A. Borsh RN, D. M. Cosgrove III, and J.-P. Yared Secular Trends in Nosocomial Bloodstream Infections in a 55-Bed Cardiothoracic Intensive Care Unit Ann. Thorac. Surg., January 1, 1998; 65(1): 95 - 100. [Abstract] [Full Text] [PDF]
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M. G. Massad and P. M. McCarthy Will permanent LVADs be better than heart transplantation? Eur J Cardiothorac Surg, April 1, 1997; 11(Supplement): S11 - S17. [Abstract] [PDF]
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W. E. Richenbacher and W. S. Pierce Mechanical Circulatory Support Ann. Thorac. Surg., November 1, 1996; 62(5): 1558 - 1559. [Full Text]
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M. G. Massad, P. M. McCarthy, N. G. Smedira, D. J. Cook, N. B. Ratliff, M. Goormastic, R. L. Vargo, J. Navia, J. B. Young, and R. W. Stewart DOES SUCCESSFUL BRIDGING WITH THE IMPLANTABLE LEFT VENTRICULAR ASSIST DEVICE AFFECT CARDIAC TRANSPLANTATION OUTCOME? J. Thorac. Cardiovasc. Surg., November 1, 1996; 112(5): 1275 - 1283. [Abstract] [Full Text]
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