intermittent pneumatic soft tissue compression: changes in periosteal and medullary canal blood flow

Intermittent Pneumatic Soft Tissue Compression:Changes in Periosteal and Medullary Canal Blood Flow

Sang-Hyun Park, Mauricio Silva

The J. Vernon Luck Sr. M.D. Orthopaedic Research Center, Orthopaedic Hospital/UCLA, 2400 S. Flower Street,Los Angeles, California 90007

Received 22 March 2007; accepted 23 July 2007

Published online in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/jor.20509

ABSTRACT: We previously demonstrated that the use of intermittent pneumatic soft tissuecompression (IPC) treatment enhanced fracture healing in an animal model, but the exactmechanism remained unknown. The purpose of this study was to determine the local andremote effects of IPC treatment on blood flow within the medullary canal and outside the periosteumof mid-tibial diaphysis. Blood flow was measured with a Laser Doppler blood flow meter in the lowerlimbs of 21 rabbits. Laser probes were inserted at three different sites of the mid-diaphysis on theright tibia: in the medullary canal (n¼ 21), outside the periosteum on the lateral side (n¼ 11), andoutside the periosteum on the medial side (n¼10). IPC was applied for 30 min through cuffs thatwere placed around the feet and the lower part of the calf. While applying IPC to the left leg, nochanges in blood flow occurred on the right leg (remote changes). However, while applying IPC to theright leg, significant localized changes were found on the right leg, including 47 and 89% increases intotal amount of blood flow outside the lateral and medial periosteum, respectively. Although analtered blood flow pattern was observed in the medullary canal, no significant change in total amountof blood flow was observed at this level. In summary, the present study demonstrated that the use ofIPC in an intact bone model results in a significant local increase in total blood flow, with minimalmeasurable effects on the contralateral limb. � 2007 Orthopaedic Research Society. Published by

Wiley Periodicals, Inc. J Orthop Res 26:570–577, 2008

Keywords: intermittent pneumatic soft tissue compression; medullary canal bloodflow; periosteal blood flow

INTRODUCTION

The use of intermittent pneumatic soft tissuecompression (IPC) has the potential of enhancingthe fracture healing process, especially for fracturesof the lower extremities. Our previous study, inwhich IPC was applied to the hind limbs of animalsthat had received a transverse tibial osteotomywith a 3-mm gap, demonstrated that daily use ofIPC for 4 weeks is associated with a significantincrease in callus area, mineral content, torsionalstiffness, and energy required to failure at theosteotomy gap.1 However, the mechanism bywhich IPC enhances fracture healing remains tobe elucidated. More than one mechanism mightresponsible for the IPC therapeutic effects, frommechanical effects producing a decrease in venousstasis to an array of chemical effects that includean increase in the synthesis of nitric oxide, prosta-cyclin, and tissue plasminogen activator, and adecrease in plasminogen activator inhibitor.

Blood circulation, especially arterial flow, is akey factor in fracture healing.2–4 The improve-ments in bone healing observed after applicationof IPC are likely related to changes in bloodflow around the fracture area. Applied to thelower extremity, a sudden application of uniform,external pressure imposes a change in its structureand hemodynamics, accelerating the blood for-ward, effectively facilitating venous emptying andpreventing stasis. The improved emptying of lowerextremity veins, with the subsequent decrease invenous pressure, leads to an increase in arterial–venous pressure gradient, ultimately resulting inan increase in arterial blood flow.5,6

Available measurements of the effects of IPCon the hemodynamics of the lower extremityhave monitored blood flow increases that occurredsystemically and in areas located proximal to theapplied compressive forces.5–7 Some data suggestthat IPC may contribute to circulatory systemiceffects by producing a significant increase in shearstresses on the endothelium of the blood vessels,leading to an increase in nitric oxide release, with aresultant induction of systemic vasodilatation.8–11

Other studies showed that application of IPC to the

570 JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2008

Correspondence to: Sang-Hyun Park (Telephone: 213-742-1443; Fax 213-742-1365; E-mail: [email protected])

� 2007 Orthopaedic Research Society. Published by Wiley Periodicals,Inc.

foot and calf can greatly enhance blood peakvelocity and flow within the popliteal vein, result-ing in an increase in arterial blood flow within thepopliteal artery.5,6,11

However, little or no knowledge exists about thelocal effects of IPC. It seems likely that local effectsof IPC, namely an increase in the blood flow at thefracture site, could be responsible for the observedenhancements in fracture repair. Our study hadtwo specific purposes: to determine local effects ofIPC by measuring the hemodynamic effects locatedat the middle aspect of the tibial shaft ipsilateral tothe treatment and to determine effects of IPC on thecontralateral limb’s blood flow, by measuring thehemodynamic effects located at the middle aspect ofthe tibial shaft contralateral to the treatment.

MATERIALS AND METHODS

Twenty-one female, skeletally mature (12–24 monthsold), New Zealand White rabbits, ranging in weight from4.1 to 5.1 kg, were maintained in accordance with aprotocol approved by the Institutional Animal Care andUse Committee.

Blood perfusion, a product of the concentration andvelocity of moving blood cells, is linearly correlatedwith the amount of blood flow.12,13 For that reason, thetotal amount of blood flow was measured using a LaserDoppler Perfusion Monitor (PF 5010, Perimed, Jarfalla,Sweden). Blood flow was measured in the middle aspectof the right tibial shaft with the animal in a supinereverse Trendelenburg position (with the treated limb atleast 20 cm below the heart level), during application ofIPC to the right (local effect) or the left hind limb (remoteeffect).

Laser Probe Implantation

Each animal was anesthetized using ketamine (40 mg/kg)and zylazine (5 mg/kg), administered subcutaneously. Theheart rate and oxygen saturation of the blood werecarefully monitored during the procedure using a Nellcorpulseoximeter (Hayword, CA). An additional dose ofanesthetics (10 mg/kg of ketamine and 1.25 mg/kg ofzylazine) was administrated to those animals in which anincrease in heart rate of at least 10% above the restingheart rate was observed. Once anesthetized, the animalwas placed in a supine position on a Plexiglas bed using acustom-made body sling, for retraining purposes. Remova-ble, molded, below-the-knee, bivalved casts, containingfour pneumatic balloons (two anteriorly and two posteri-orly), were applied to both hind limbs prior to implantationof the probes (Fig. 1).

To maintain a steady position of the right limb andto minimize relative motion that could affect blood flowmeasurements, the right limb was firmly attached to thePlexiglas bed. For this purpose, a custom-made boneclamp was attached, transcutaneously, to the medial and

lateral aspects of the right tibial plateau. The heel ofthe bivalved casts was fixed to the Plexiglas bed usinga Velcro band, immobilizing the knee at about 458 offlexion.

Two 20-gauge spine needles (OD¼ 0.9 mm) were usedas insertion guides for the Laser Doppler probes. Theneedles were inserted percutaneously and located atthe level of the middle third of the tibial shaft, either inthe medullary canal or outside the periosteum. In allanimals (n¼ 21), a guide was inserted in the canal of theright tibial shaft. A 0.9-mm hole was drilled on the medialside of the proximal cortex, through which the guide wasinserted and advanced, reaching the middle aspect of theshaft. In half the animals (n¼ 11), one guide was insertedjust outside the periosteum on the lateral side of theshaft, and in the remaining half (n¼ 10) one guide wasinserted just outside the periosteum on the medial side ofthe shaft (Fig. 2).

After placing the guide needles, 0.5-mm diameterLaser Doppler fiber optic probes (MT B500, Perimed,Jarfalla, Sweden) were inserted through them. To avoidbleeding caused by the insertion of the probes, carefulattention was given to extrude the tip of the probe nomore than 3 mm deeper than the tip of the guide needle.

Figure 1. A removable bivalved cast held four pneumaticballoons that were placed around the lower hind limbs, twoanteriorly and two posteriorly, with two over the foot and twoover the lower part of calf. Lower graph shows the pressureprofile of the balloons. Arrows indicate position of the tibia andlaser probes.

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JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2008

After insertion, the probes were connected to a LaserDoppler Perfusion Monitor (PF 5010, Perimed, Jarfalla,Sweden).

IPC Treatment

IPC was applied using a modified ArterialFlow system32A (Aircast, Inc., Summit, NJ), following a previouslydescribed protocol.1 The modified system allows forrapid, graduated, and sequential (distal to proximal)compression. The distal pneumatic rubber balloonsinflate rapidly, reaching 95 mmHg, and the proximalpneumatic balloons follow in 0.3 s to reach 85 mmHg.After 2 s of compression, both sets of balloons deflate,with a noncompression period of 17 s (Fig. 1). IPC wasapplied to the right hind limb (local effect) or the lefthind limb (remote effect).

Blood Flow Measurement

In vivo assessments of changes in blood perfusion at themiddle aspect of the right tibial shaft, as measured byblood flow, were performed continuously with a LaserDoppler Perfusion Monitor (PF 5010, Perimed, Jarfalla,

Sweden), following a specific sequence (Table 1). Allmeasurements were made with the animal in a 308reverse Trendelenburg position, to locate the measure-ment site 20 cm below the heart level. Once in thatposition, an initial resting period of 20 min was allowedto obtain hemodynamic equilibrium. After equilibriumwas obtained, IPC was applied to the left hind limb for30 min. A 20-min resting period was then observed toreturn to equilibrium. Then, IPC was applied to theright hind limb for 30 min. Finally, a 20-min restingperiod allowed return to equilibrium.

Although blood flow was measured continuously, thetotal amount of blood flow per compression/resting cycle(20 s), the high peak blood flow, and the low peak bloodflow were measured at five time points: just before start ofIPC, at 10, 20, and 30 min after start of IPC, and after20 min of resting. The blood flow analysis during the 20-scompression/resting sequence was further divided intotwo stages: during the 3-s cuff compression period, andduring the 17-s noncompression period (Fig. 3).

Blood flow data obtained during IPC application to theleft hind limb was compared to the hemodynamicequilibrium value obtained in the reverse Trendelenburgposition, immediately before IPC treatment to the lefthind limb. Changes in blood flow data observed duringthis time period were considered remote IPC effects.Blood flow data obtained during the application of IPC tothe right hind limb was compared to the hemodynamicequilibrium value obtained immediately before applica-tion of IPC to the right hind limb. Changes in blood flowdata observed during this period of time were consideredlocal IPC effects.

Statistical Analysis

A paired Student t-test was used to calculate thesignificance level of remote and local effects of IPC. Ap-value <0.05 was considered significant.

RESULTS

Remote Effects of IPC Treatment

IPC treatment on the left hind limb resulted in nonoticeable changes in the pattern of pulsatile flowor the total amount of blood flow on the right hindlimb. The total amount, high peak blood flow, and

Figure 2. Radiographs showing the position of the laser probeguide needles. (A) Guide needles inserted outside the periosteumon the lateral side of the tibial shaft and inside the medullarycanal. (B) Guide needles placed outside the periosteum on themedial side of the tibial shaft and inside the medullary canal.The tip of the laser probe was protruding 3 mm outside of theguide needle.

Table 1. Experimental Design: Blood Flow Measurement Sequence

MeasurementSequence Body Position IPC Treatment Duration Reference

1 Horizontal No 10 min2 Reverse Trendelenburg No 20 min Equilibrium value for remote effect3 Reverse Trendelenburg Contralateral Left limb 30 min4 Reverse Trendelenburg No 20 min Equilibrium value for local effect5 Reverse Trendelenburg Ipsilateral Right limb 30 min6 Reverse Trendelenburg No 20 min

Blood flow was monitored only from the right hind limb.

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low peak blood flow in the medullary canal of theright tibias were nearly constant throughout IPCtreatment (Fig. 3). The periosteal blood flow onthe right tibia decreased gradually during IPCtreatment to the left hind limb. These changeswere observed over time at both sides of theperiosteum, but were more severe on the medialside (Fig. 4). These changes in periosteal bloodflow were not reversed once IPC treatment wasdiscontinued, with a persistent drop in blood flowduring the resting period.

Local Effects of IPC

IPC treatment on the right limb resulted insignificant changes in both the pattern of pulsatileflow of the right limb and the total amount ofblood flow. The changes in blood flow observedat the medullary canal were different than thoseobserved at periosteum (Fig. 3). The pattern ofblood flow outside the periosteum increased rapi-dly during the inflation of both proximal and distalpneumatic cuffs. This initial blood flow increasewas followed by a rapid decrease during the 2-s

compression period and a secondary increase justafter deflation of the cuffs (Fig. 3).

The total amount of blood flow at the periosteumincreased during the 20-s compression/restingcycle, with a maximum increase in total amountof blood flow of 89% (p¼ 0.02) and 47% (p¼ 0.002)over the medial and lateral sides of the periosteum,respectively, 10 min after the start of IPC treat-ment (Fig. 5). This increase in the total amount ofblood flow was sustained throughout the 30-minIPC treatment period. The values of total amountof blood flow returned to normal after the 20-minresting period.

The total amount of blood flow during the 20-scompression/resting sequence was further ana-lyzed during the 3-s cuff compression period andthe 17-s noncompression period. During the 3-speriod, the total amount of blood flow increasedon both sides of the periosteum. The maximumincrease was observed 10 min after the start ofIPC treatment, with an increase in total amountof blood flow of 365% on the medial side of theperiosteum (p¼ 0.0002), and 334% on the lateralside of the periosteum (p¼ 0.009). During this

Figure 3. Blood flow profiles during two IPC cycles, inside the medullary canal and outside theperiosteum.



period both the high and low peak blood flowvalues increased. The maximum increase in highpeak blood flow was observed 10 min after thestart of IPC treatment, with an increase of 607%

( p¼ 0.0001). The maximum increase in low peakblood flow was observed 30 min after the start ofIPC, with an increase of 76% (p¼ 0.01). During the17-s noncompression period, the total amount of

Figure 4. The periosteal blood flow on the right tibia decreased gradually during the IPCtreatment to the left hind limb, suggesting no effect of IPC treatment on the blood flow of thecontralateral limb.

Figure 5. Total amount of blood flow changeduring the 20-s compression/restingcycle on the righthind limb, demonstrating local effects of IPC treatment.

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blood flow also increased on both sides of theperiosteum, although to a lesser extent. Themaximum increase was observed 10 min after thestart of IPC, with an increase in total amount ofblood flow of 20% on both the medial and lateralsides of the periosteum (p¼ 0.04 and p¼ 0.006,respectively) (Fig. 6).

The effect of the IPC treatment on the totalamount of blood flow inside the medullary canalwas minimal. The pattern of blood flow inside themedullary canal was not affected by the inflationof the distal pneumatic cuffs, but demonstrated arapid decrease, even below baseline levels, duringthe inflation of the proximal cuffs. The pattern ofblood flow increased above baseline levels just afterthe deflation of the pneumatic cuffs (Fig. 3).

The total amount of blood flow inside themedullary canal during the 20-s compression/resting cycle remained almost constant, with amaximum increase in total amount of blood flow ofonly 2% during IPC treatment (p¼ 0.35) (Fig. 5).During the 3-s cuff compression period, however,the high and low blood flow values inside themedullary canal moved away from baseline, witha maximum increase in high peak blood flow(19%, p¼ 0,003) and a maximum decrease in lowpeak blood flow both observed 10 min after the startof IPC (25%, p¼ 0.0004). During the 17-s non-compression period the total amount of blood flow

inside the medullary canal remained nearly con-stant (Fig. 6), with a maximum increase in totalamount of blood flow of only 3% during IPCtreatment (p¼ 0.21).

DISCUSSION

Devices that provide intermittent, pneumaticsoft-tissue compression have been widely used inthe field of orthopedics.1,5,14,15 Our previous study,in which IPC was applied to the hind limbs ofanimals that had received a transverse tibialosteotomy with a 3-mm gap, demonstrated thatIPC also has the potential to enhance fracturehealing.1 In that study, osteotomies treated withIPC exhibited 27% larger callus area and 50%higher mineral content than control osteotomiesat 6 weeks. The torsional stiffness, maximumtorque, angular displacement at maximum torque,and energy required to failure of specimens inthe study group were 27, 62, 36, and 111% higher,respectively, than those in the control group at8 weeks.1

Results of previous studies demonstratedsystemic circulatory effects after the applicationof IPC to both lower extremities, either by inducingsystemic vasodilatation8–11 or by enhancing bloodflow.5,6,16,17 However, limited knowledge existswith regard to the local hemodynamic effects of

Figure 6. Total amount of blood flow change during the 17-s noncompression period, indicating aresidual effect of soft tissue compression on blood hemodynamics.



IPC. To our knowledge, available measurements ofblood flow associated with IPC have been obtainedin distant areas, proximal to the compressioncuffs.5,6,8–11,16–18 With such measurements, it isimpossible to determine the exact anatomic loca-tion where these changes are being originated andthe anatomical areas that are being bypassed in theprocess, which would be essential informationwhen considering specific effects of IPC on fracturehealing.

The results of this study demonstrate that IPCcan result in a significant local increase inpeak and total amount of blood flow. These changeswere observed outside the periosteal tissue,with minimal changes within the medullary canal.The increases in total blood flow slowly disappearedduring the 17-s noncompression period. At theperiosteal level, the initial increase in blood flowmight indicate a rapid emptying of blood vesselsduring soft-tissue compression, with a secondaryincrease in blood flow due to a rapid refilling of theempty vessels during the resting period. A signifi-cant increase in blood flow to the fracture site wouldprobably improve the supply of essential elementssuch as growth hormone, calcium, amino acids,proteins, growth factors, oxygen, and other compo-nents necessary for fracture repair. The observedlocal increase in periosteal blood flow might beresponsible for the enhancement in external callusformation associated with IPC treatment describedin our previous study.1

Previous studies have suggested that IPC treat-ment can result in systemic hemodynamic effects,probably due to strong shear stresses on thevascular endothelium and the subsequent releaseof potent vasodilators like nitric oxide.8–11 Inthe present study, no remote hemodynamic effectswere observed in association with IPC treatment. Apossible explanation is the fact that we measuredthe remote hemodynamic effects of IPC treatmentin the noncompressed, contralateral hindlimb ofthe experimental animals. To our knowledge, allprevious measurements of the systemic effects ofIPC have been made in blood vessels locatedproximal to the bifurcation of the iliac arteries andveins8–11 in animals that received IPC simulta-neously in both hindlimbs. A sudden application ofsoft tissue compression in the hind-limb, as providedby the pressure cuff in the IPC treatment, mightresult in a dual mechanical effect: a sudden arterialstasis and an increase in venous blood volume invessels proximal to the pressure cuffs, both of whichwould result in proximal vessel dilation withoutnecessarily being associated with a chemical effector representing a true systemic effect. The small

effective area of soft tissue compression, as providedby the pressure cuffs in this study, is probablyinsufficiently large togenerateadequate endothelialshear stresses and, therefore, to release enoughchemical agents to produce a generalized dilation.Further studies on the systemic effects of IPC, withspecific measurements of vasoactive agents, arerequired.

In the present study, the use of IPC induceda different response in the medial side of theperiosteum compared to the lateral side. A consi-derably higher increase in total blood flow wasobserved over the medial side of the periosteum,which could be explained by the fact that perio-steum located on the medial side of the tibia isnot covered with thick muscular groups. It islikely that, before IPC treatment, the total amountof blood flow over the lateral aspect of the perio-steum is higher due to the compression providedby muscle contraction (muscle pump). Once IPCis started, the blood flow imbalance betweenthe medial and lateral sides of the periosteum iscompensated by the symmetric contractions of thecompression cuffs, resulting in a relatively higherincrease in blood flow over the medial side of theperiosteum. In addition, the lack of muscle cove-rage over the medial side of the tibia probablyallows a more effective direct compression of theblood vessels by the pressure cuffs.

This study has limitations. The laser probes usedfor the measurements of blood are very sensitive,scanning an area of about 0.5 mm in diameter and0.5 mm in depth. Therefore, the distribution anddensity of blood vessels around the tip of the probeis critical for blood flow measurement. Because theprobes are inserted percutaneously, the position ofthe probe might not be the same in all animals,and the density of blood vessels among subjects isdifferent. As a result, blood flow measurementsmight differ between study subjects. To minimizethis factor, we normalized all blood flow values tothe value of hemodynamic equilibrium, thereforeeliminating actual differences between subjects.The blood flow measurements obtained in thepresent study cannot be extrapolated to measure-ments obtained in a fracture model. The patternsand total amounts of blood flow, both in themedullary canal and in the periosteum, mightdiffer considerably in the presence of a fracture andduring the healing process. Without a fracture, themedullary canal is protected from external com-pression by an intact cortical shell. Compression tothe soft tissues surrounding the intact bone isprobably not enough to produce significant changesin the blood flow inside the canal. In the presence of

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a fracture, effective compression of surroundingtissues might result in pressure gradients insidethe canal, altering the patterns and amounts ofblood flow. Further studies of the effects of IPCtreatment in blood flow in a fracture model areguaranteed.

In summary, the present study demonstratedthat the use of intermittent pneumatic soft-tissuecompression in an intact bone model results in asignificant local increase in total blood flow,with minimal measurable effects on the blood flowof the contralateral limb.

ACKNOWLEDGMENTS

This study was supported by the Los Angeles Ortho-paedic Hospital Foundation and Aircast LLC.

REFERENCES

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2. Cornell CN, Lane JM. 1992. Newest factors in fracturehealing. Clin Orthop Relat Res 277:297–311.

3. Rhinelander FW. 1968. The normal microcirculation ofdiaphyseal cortex and its response to fracture. J Bone JointSurg Am 50-A:784–800.

4. Rhinelander FW. 1974. Tibial blood supply in relation tofracture healing. Clin Orthop 105:34–81.

5. Delis KT, Labropoulos N, Nicolaides AN, et al. 2000. Effectof intermittent pneumatic foot compression on poplitealartery haemodynamics. Eur J Vasc Endovasc Surg 19:270–277.

6. Delis KT, Slimani G, Hafez HM, et al. 2000. Enhancingvenous outflow in the lower limb with intermittentpneumatic compression. A comparative haemodynamicanalysis on the effect of foot vs. calf vs. foot and calfcompression. Eur J Vasc Endovasc Surg 19:250–260.

7. Delis KT, Nicolaides AN, Wolfe JH. 2001. Peripheralsympathetic autoregulation in arterial calf inflow en-hancement with intermittent pneumatic compression.Eur J Vasc Endovasc Surg 22:317–325.

8. Chen LE, Liu K, Qi WN, et al. 2002. Role of nitric oxidein vasodilation in upstream muscle during intermittentpneumatic compression. J Appl Physiol 92:559–566.

9. Liu K, Chen LE, Seaber AV, et al. 1999. Intermittentpneumatic compression of legs increases microcirculationin distant skeletal muscle. J Orthop Res 17:88–95.

10. Liu K, Chen LE, Seaber AV, et al. 1999. Influencesof inflation rate and duration on vasodilatory effect byintermittent pneumatic compression in distant skeletalmuscle. J Orthop Res 17:415–420.

11. Zhang L, Looney CG, Qi WN, et al. 2003. Reperfusioninjury is reduced in skeletal muscle by inhibition ofinducible nitric oxide synthase. J Appl Physiol 94:1473–1478.

12. Heden P, Jurell G, Arnander C. 1986. Prediction of skinflap necrosis: a comparative study between laser Dopplerflowmetry and fluorescein test in a rat model. Ann PlastSurg 17:485–488.

13. Perbeck L, Lindquist K, Proano E, et al. 1990. Correlationbetween fluorescein flowmetry and laser Doppler flowme-try. A study in the intestine (ileoanal pouch) in man. ScandJ Gastroenterol 25:520–524.

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15. Warwick D, Harrison J, Whitehouse S, et al. 2002. Arandomised comparison of a foot pump and low-molecular-weight heparin in the prevention of deep-vein thrombosisafter total knee replacement. J Bone Joint Surg [Br] 84-B:344–350.

16. Delis KT, Husmann MW, Cheshire NJ, et al. 2001.Effects of intermittent pneumatic compression of the calfand thigh on arterial calf inflow: a study of normals,claudicants, and grafted arteriopaths. Surgery 129:188–195.

17. Lurie F, Awaya DJ, Kistner RL, et al. 2003. Hemodynamiceffect of intermittent pneumatic compression and theposition of the body. J Vasc Surg 37:137–142.

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intermittent pneumatic soft tissue compression: changes in periosteal and medullary canal blood flow

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