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Ann Thorac Surg 2007;84:568-573
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Blood Flow Changes in Normal and Ischemic Myocardium During Topically Applied Negative Pressure

Sandra Lindstedt, MDa,*, Malin Malmsjö, MD, PhDb, Richard Ingemansson, MD, PhDa

a Department of Cardiothoracic Surgery, Lund University Hospital, Lund, Sweden
b Department of Medicine, Lund University Hospital, Lund, Sweden

Accepted for publication February 22, 2007.

* Address correspondence to Dr Lindstedt, Department of Cardiothoracic Surgery, Heart and Lung Center, Lund University Hospital, SE-221 85 Lund, Sweden (Email: sandra.lindstedt{at}skane.se).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Topical negative pressure (TNP) therapy has been adopted as a first-line treatment for wound healing. One of the mechanisms by which TNP improves healing is by stimulating blood flow to the wound edge. Among patients with ischemic heart disease, it is of great importance to improve the microvascular blood flow in the myocardium during episodes of ischemia to protect the myocardium from infarction. The present study was designed to elucidate the effect of TNP on microvascular blood flow in the myocardium.

Methods: Six pigs underwent median sternotomy. The microvascular blood flow in the myocardium was recorded, before and after the application of TNP, by using laser Doppler velocimetry. Analyses were performed before left anterior descending artery (LAD) occlusion (normal myocardium), after 20 minutes of LAD occlusion (ischemic myocardium), and after 20 minutes of reperfusion (reperfused myocardium).

Results: TNP at –0 mm Hg increased microvascular blood flow in the normal myocardium from 14.7 ± 3.9 perfusion units (PU) before to 25.8 ± 6.1 PU after TNP application (p < 0.05), in the ischemic myocardium from 7.2 ± 1.5 PU before to 13.8 ± 2.6 PU after TNP application (p < 0.05), and in the reperfused myocardium from 10.8 ± 2.0 PU before to 19.3 ± 5.6 PU after TNP application (p < 0.05).

Conclusions: TNP increases the microvascular blood flow significantly in normal, ischemic, and reperfused myocardium and may provide a novel therapeutic tool in the treatment of ischemic myocardium.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Topical negative pressure (TNP) has been shown to facilitate the healing of chronic and problematic wounds, including diabetic wounds [1], burn wounds [2], and poststernotomy mediastinitis [3–5]. One mechanism by which TNP promotes wound healing is by stimulating wound edge blood flow, as has been demonstrated in peripheral [6] and in skeletal muscle in sternotomy wounds [7, 8]. TNP produces mechanical stress and a pressure gradient across the tissue, which may cause a surge of blood to the area [6, 9–11]. Mechanical forces and increased blood flow are known to stimulate endothelial proliferation, capillary budding, and angiogenesis [12].

In ischemic heart disease, therapeutic interventions such as percutaneous coronary intervention (PCI) and coronary artery bypass grafting surgery (CABG) are performed to improve blood flow to the ischemic myocardium. These treatments are successful in most cases, although such interventions are not possible for patients with refractory angina pectoris because of extensive coronary vessel disease. Percutaneous myocardial laser revascularization [13, 14] and enhanced external counterpulsation [15, 16] have been tried with varying results [17]. A means of increasing microvascular blood flow in the ischemic myocardium would thus be beneficial.

TNP is known to stimulate blood flow in various tissues [6], including the skeletal muscle [7, 8]. We conducted this study to examine the effects of TNP on microvascular blood flow in normal, ischemic, and reperfused myocardium. Blood flow was measured using laser Doppler velocimetry in a porcine model. The effect of TNP on microvascular blood flow was investigated in the myocardium before, during, and after occlusion of the left anterior descending artery (LAD).


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Experimental Animals
A porcine model was use for the present study. Six domestic Landrace pigs of both genders (mean body weight, 70 kg) were fasted overnight with free access to water. The study was approved by the Ethics Committee for Animal Research, Lund University, Sweden. The investigation complied with the Guide for the Care and Use of Laboratory Animals (US National Institutes of Health, National Academies Press; 1996).

Anesthesia
The animals were premedicated intramuscularly with ketamine (30 mg/kg) before they were brought into the laboratory. Before the procedure began, sodium thiopental (5 mg/kg), atropine (0.02 mg/kg), and pancuronium (0.5 mg/kg) were given intravenously. A tracheotomy was performed with a Portex endotracheal tube (7.5 mm internal diameter, Smiths Medical, Carlsbad, CA) A servo-ventilator (Siemens Elema 300A, Stockholm, Sweden) was used for mechanical ventilation throughout the experiment. The ventilator settings were minute volume, 100 mL/kg; fraction of inspired oxygen, 0.5; breathing frequency, 16 breaths/min; and positive end expiratory pressure, 5 cm H2O.

Anesthesia and muscular paralysis were maintained with a continuous intravenous infusion of 8 to 10 mg/(kg · hour) propofol (Diprivan, AstraZeneca, Södertälie, Sweden), 0.15 mg/(kg · hour) fentanyl (Leptanal, Lilly, Suresnes, France), and 0.6 mg/(kg · hour) pancuronium (Pavulon, Organon Teknika, Boxtel, The Netherlands).

Mean arterial pressure, central venous pressure, heart frequency, and ventilatory measurements were recorded throughout the experiments.

Surgical Procedure
The procedure was performed through median sternotomy. After heparinization (400 IU/kg), cardiopulmonary bypass (CPB) was initiated with a 22F arterial cannula (DLP, elongated one-piece arterial cannula, Medtronic Inc, Minneapolis, MN) in the distal ascending aorta, and a 32F venous cannula (MC2 two-stage venous cannula, Medtronic, Inc) inserted through the right atrium. Before cannulation of the heart, the cannulas were inserted through the thoracic wall to prevent air leakage during TNP application. CPB was conducted in normothermia. Ventricular fibrillation was subsequently induced in the heart.

No aortic cross-clamping was performed, and no cardioplegia was used. The mean arterial pressure was maintained between 60 and 80 mm Hg. A left ventricular vent (DLP Vent, Medtronic Inc) was used to protect the left chamber from overloading. Pulmonary ventilation was applied at a rate of 4 L/min during the experiments.

CPB was used to facilitate the measurements of microvascular blood flow using laser Doppler velocimetry. Fibrillation of the heart minimizes the movement artifacts, while the physiologic conditions are largely conserved. Moreover, CPB prevents the risk of circulatory failure during LAD occlusion, thereby facilitating experimental analysis in the case of the ischemic myocardium.

Microvascular blood flow was measured with laser Doppler velocimetry (Transonic Laser Doppler Monitor, BLF21, Maastricht, The Netherlands) by using a technique that quantifies the sum of the motion of the red blood cells in a specific volume. This method, which is extensively applied in plastic surgery procedures [18], uses a fiberoptic probe carrying a beam of light. Light impinging on cells in motion undergoes a change in wavelength (Doppler shift), and light impinging on static objects remains unchanged. The magnitude and frequency distributions of the changes are directly related to the number and velocity of red blood cells. The information is collected by a returning fiber, converted into an electronic signal, and analyzed.

Laser Doppler probes were inserted horizontally into the heart muscle 8 to 10 mm lateral of the LAD at depths of approximately 6 to 8 mm. All probes were carefully fixed to the surface of the heart with a Prolene 7-0 suture (Ethicon Inc, Somerville, NJ), thereby preventing probe movement. After the experiments, the heart was dissected and the probe location was confirmed (Fig 1).


Figure 1
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  		Fig 1. As shown in this photograph, the laser Doppler probes were inserted horizontally into the heart muscle 8 to 10 mm lateral of the left anterior descending artery (LAD); that is, the septum of the heart, at depths of approximately 6 to 8 mm. The photograph also shows the location of right coronary artery (RCA).

 
A round hole 5 cm in diameter was made in the middle of a phrenic nerve pad (Medtronic Inc) and placed on top of the heart. The pad was stabilized by 8 to 10 Prolene 5-0 sutures to the surrounding myocardium and by Dermalon 2-0 sutures (Syneture, Norwalk, CT) the posterior sternal edges. A retractor was used throughout the experiments to keep the sternal edges apart. A polyurethane foam dressing with an open pore structure of 400 to 600 µm (KCI, Copenhagen, Denmark) was placed between the sternal edges. The foam was continuously sutured to the surrounding skin with Dermalon 2-0. The wound was sealed with a transparent adhesive drape.

A Track Pad (KCI) was inserted through the drape and was connected to a vacuum pump, (V.A.C. pump unit, KCI). When the negative pressure is applied, the heart is drawn up towards the phrenic nerve pad and the foam without interfering with the sternal edges. This procedure causes the application of negative pressure to affect only the myocardium exposed by the 5 cm diameter hole.

Experimental Protocol
The microvascular blood flow was measured continuously by the laser Doppler filament probes. Recordings were made in normal myocardium before a –50 mm Hg pressure was applied and immediately after the negative pressure was turned off.

The LAD was occluded for 20 minutes with an elastic vessel loop. Microvascular blood flow was then measured before and after 1, 5, 10, 15, and 20 minutes of occlusion. A negative pressure of –50 mm Hg was then applied to the heart, and microvascular blood flow changes were recorded. The negative pressure was then removed.

The LAD occlusion was released and microvascular blood flow was measured before and after 1, 5, 10, 15, and 20 minutes of reperfusion. A negative pressure of –50 mm Hg was then applied to the heart, and microvascular blood flow changes were measured. The negative pressure was then removed.

Calculations and Statistics
Laser Doppler velocimetry measurements were performed on 6 pigs. The output was continuously recorded using PeriSoft software (Perimed, Stockholm, Sweden). Microvascular blood flow was expressed in terms of perfusion units (PU). Calculations and statistical analysis were performed using GraphPad 4.0 software (GraphPad Software, San Diego, CA). Statistical analysis was performed using Student paired t test. Significance was defined as p < 0.05. Values are presented as means ± the standard error of the mean.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Normal Myocardium
A topical negative pressure of –50 mm Hg induced an immediate significant increase in microvascular blood flow in normal myocardium from 14.7 ± 3.9 PU before to 25.8 ± 6.1 PU after TNP application (p < 0.05; Fig 2). When the vacuum pump was switched off, the blood flow returned to baseline values of 13.3 ± 2.4 PU.


Figure 2
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  		Fig 2. Microvascular blood flow measured in normal myocardium using laser Doppler velocimetry. The measurements were performed at a depth at 6 to 8 mm in the myocardium in 6 pigs, with a topical negative pressure of –50 mm Hg (grey bar) compared with no negative pressure (open bar). The results are shown in blood flow perfusion units (PU) as mean values ± standard error of the mean (*p < 0.05). The right panel shows a representative example of microvascular blood flow changes after the application of –50 mm Hg topical negative pressure before left anterior descending artery occlusion (normal myocardium). Note the immediate blood flow response when the negative pressure is applied.

 
Ischemic Myocardium
Ischemia was induced by occlusion of the LAD for 20 minutes. The myocardium distal to the occlusion turned blue, indicating that ischemia of the myocardium had been established. The blood flow was 12.8 ± 2.6 PU before occlusion of the LAD and decreased to 7.2 ± 1.5 PU (p < 0.01) after 20 minutes of LAD occlusion (Fig 3). Upon application of a topical negative pressure of –50 mm Hg, an immediate significant increase in blood flow was seen in the ischemic myocardium from 7.2 ± 1.5 PU before to 13.8 ± 2.6 PU after TNP application (p < 0.05; Fig 4).


Figure 3
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  		Fig 3. Microvascular blood flow measured using laser Doppler velocimetry in the myocardium before and after 20 minutes of left anterior descending artery (LAD) occlusion. Note the significant decrease from 12.8 ± 2.6 perfusion units (PU) to 7.2 ± 1.5 PU in microvascular blood flow in the area after LAD occlusion. The results are shown as mean values ± standard error of the mean (*p < 0.05).

 

Figure 4
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  		Fig 4. Microvascular blood flow measured during occlusion using laser Doppler velocimetry in ischemic myocardium. The measurements were performed at a depth at 6 to 8 mm in the myocardium in 6 pigs, with a topical negative pressure of –50 mm Hg (grey bar) compared with 0 pressure (open bar). In the left pane, the results in blood flow perfusion units (PU) are shown as mean values ± standard error of the mean (*p < 0.05). The right panel shows a representative example of microvascular blood flow changes after the application of –50 mm Hg topical negative pressure after 20 minutes of left anterior descending artery occlusion (ischemic myocardium). Note the immediate blood flow response when the negative pressure is applied.

 
Reperfused Myocardium
The LAD occlusion was then released and the blue ischemic myocardium turned red, indicating reperfusion. After 20 minutes of reperfusion, the application of –50 mm Hg induced an immediate significant increase in blood flow from 10.8 ± 2.0 PU before to 19.3 ± 5.6 PU after TNP application (p < 0.05; Fig 5).


Figure 5
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  		Fig 5. Microvascular blood flow measured using laser Doppler velocimetry in ischemic myocardium during reperfusion. The measurements were performed at a depth at 6 to 8 mm in the myocardium in 6 pigs with a topical negative pressure of –50 mm Hg (grey bar) compared with 0 pressure (open bar). In the left panel, the results in perfusion units (PU) are shown as mean values ± standard error of the mean (*p < 0.05). The right panel shows a representative example of microvascular blood flow changes after application of –50 mm Hg topical negative pressure after 20 minutes of LAD occlusion, followed by 20 minutes of reperfusion (reperfused myocardium). Note the immediate blood flow response when negative pressure is applied.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Among patients with ischemic heart disease, it is of great importance to improve the microvascular blood flow in the myocardium during episodes of ischemia to protect the myocardium from infarction. Today, many different drugs and sophisticated techniques such as PCI and CABG are used with remarkable results [19]. Despite this, there is a large group of patients who have been heavily treated with different drugs (leading to drug-resistant angina pectoris) who have already undergone one or more PCIs or CABG, or both, and who still have serious ischemic heart disease, also called refractory angina pectoris. Among the many different therapies that have been tried [17] are percutaneous myocardial laser revascularization [13, 14] and enhanced external counterpulsation [15, 16], with varying results. A satisfactory mode of treatment for these patients has yet to be found.

Poststernotomy mediastinitis is a rare but serious and potentially lethal complication after cardiac surgery. Conventional treatment involves surgical revision with open dressings, closed irrigation, or reconstruction with vascularized soft tissue flaps, such as omentum or pectoral muscle. Recently, TNP has become the therapy of choice for mediastinitis because of the excellent clinical outcome [5]. TNP involves subatmospheric pressure application over the wound by controlled suction through a porous dressing.

Despite the extensive clinical use and excellent outcome of TNP in wound therapy, the fundamental scientific mechanism is, to a large extent, unknown. One of the known effects of TNP is enhanced blood flow to the wound edge, as has been shown in a sternotomy wound model [7]. TNP increases blood flow velocity and opens up the capillary beds [6, 10]. Mechanical forces exerted by TNP and increased blood flow affect the cytoskeleton in the vascular cells and stimulate granulation tissue formation, which involves endothelial proliferation, capillary budding, and angiogenesis [12].

In the present study, we hypothesized that the application of TNP on the surface of the heart would stimulate microvascular blood flow in the myocardium, as seen in skeletal muscle during TNP. Indeed, we have observed that patients with poststernotomy mediastinitis treated with TNP develop a thick layer of well-vascularized granulation tissue on the exposed surface of the heart.

Mediastinitis is a strong predictor of poor long-term survival after CABG [20–25], and it has been suggested that mediastinitis may cause negative, long-term effects on several organs, such as the heart and kidneys. Of interest was a recently published study that showed no difference in long-term survival between isolated CABG patients with TNP-treated mediastinitis and CABG patients without mediastinitis [26]. Because the topical negative pressure is in direct contact with the heart, which is exposed through the diastase of the sternotomy in patients with poststernotomy mediastinitis during TNP, increased coronary collateral blood vessels may have developed during TNP and these patients might therefore be better prepared when bypass grafts fail to work.

The present study provides interesting new information on how topically applied negative pressure may improve microvascular blood flow in the myocardium. When the area of the myocardium studied was exposed to a topical negative pressure of –50 mm Hg, an immediate significant increase in microvascular blood flow was observed. This is in accordance with previous results showing increased microvascular blood flow of the skeletal muscle upon application of TNP [7, 8, 27].

To investigate whether similar results could be obtained in an ischemic model, the LAD was occluded for 20 minutes. It is commonly accepted that 20 minutes of LAD occlusion establishes ischemia in the myocardium. When the ischemic area of the myocardium was exposed to a topical negative pressure of –50 mm Hg, an immediate significant increase in microvascular blood flow was detected. Furthermore, after 20 minutes of reperfusion, myocardial blood flow significantly increased when –50 mm Hg was applied.

Increasing blood flow to the myocardium is the aim of any form of treatment of ischemic heart disease. For most patients, commonly used interventions such as PCI and CABG are successful. In patients with refractory angina pectoris, no satisfactory therapy yet exists. TNP stimulation of myocardial blood flow may be a possible therapeutic intervention. It is believed that the sheering forces exerted by TNP stimulate angiogenesis [8, 11, 12, 28]. We have indeed observed in patients treated with TNP that richly vascularized granulation tissue develops over the heart within 4 to 5 days. These newly formed blood vessels may provide collateral blood supply that is needed when the native circulation fails to provide sufficient blood flow. It may be that the TNP stimulation of blood flow and development of collateral blood vessels in part accounts for the reduced long-term mortality in patients treated with TNP for poststernotomy mediastinitis after CABG [5, 26].

A negative pressure of –50 mm Hg was used in the present study. Blood flow stimulation by TNP has been found to be a function of tissue density, the negative pressure applied, and the distance from the wound edge [7, 28]. The most commonly used negative pressures of –75 mm Hg and –125 mm Hg stimulate blood flow to a depth of 25 mm in the skeletal muscle, whereas lower negative pressures such as –50 mm Hg stimulate blood flow closer to the surface [7]. The laser Doppler probes were placed at a depth of approximately 6 to 8 mm. To stimulate blood flow this close to the surface of the tissue, the lower negative pressure of –50 mm Hg was used.

CPB was used to minimize movement artifacts while measuring blood flow in the myocardium using laser Doppler technology. The effect of TNP on the beating heart can not be deduced from the present results, although we believe that the effect would be similar to that observed here. Furthermore, CPB facilitated the intervention because arrhythmia and circulatory failure were avoided during the induction of ischemia and reperfusion.

In this study, we applied TNP to the myocardium and showed that a topical negative pressure of –50 mm Hg causes a significant increase in microvascular blood flow, not only in normal and ischemic myocardium but also in ischemic myocardium during reperfusion. TNP may thus constitute an alternative therapeutic intervention to stimulate blood flow in the failing myocardium in patients with refractory angina pectoris. Extended preclinical trials and clinical studies on humans will be required before any clinical recommendations can be made.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We would like to thank Johan Ingemansson and Kristoffer Peters (Statistical Solutions IP) for their expert contribution to the statistic analyses. This study was supported by Anders Otto Swärd’s Foundation/Ulrika Eklund’s Foundation, Anna Lisa and Sven Eric Lundgren’s Foundation for medical research, the Åke Wiberg Foundation, the M. Bergvall Foundation, the Swedish Medical Association, the Royal Physiographic Society in Lund, the Swedish Medical Research Council, the Crafoord Foundation, the Swedish Heart-Lung Foundation, the Swedish Government Grant for Clinical Research, and the Swedish Hypertension Society.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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