1990 - Slife - Pulmonary Arterial Compliance at Rest and Exercise in Normal Humans

8/13/2019 1990 - Slife - Pulmonary Arterial Compliance at Rest and Exercise in Normal Humans

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Pulmonary arterial complianceat rest and exercise in normal humans

DAVID M. SLIFE, RICKY D. LATHAM, PIETER SIPKEMA, AND NICO WESTERHOFCardiology Service and Department of Clinical Investigation, Brooke Army Medical Center,Fort Sam Houston, Texas 78234; and Laboratory for Physiology,Free University, 1081 BT Amsterdam, The Netherlands

SLIFE, DAVID M., RICKY D. LATHAM, PIETER SIPKEMA, ANDNICO WESTERHOF. Pulmonary arterial compliance at rest andexercise in normaL humans. Am. J. Physiol. 258 (Heart Circ.Physiol. 27): H.1823-H1828, 1990.-We evaluated the feasibil-it y of determining pulmonary arterial compliance (C,) by aparameter estimation procedure based on the three-elementwindkessel model. Eight normal patients studied with multis-ensor micromanometry technology had simultaneous rest andexercise pulmonary artery pressures (PAP) and flows recorded.These were submitted to the model and independent methodsto determine C,, pulmonary characteristic impedance (Z,), andpulmonary vascular resistance (PVR). Significant changes inheart rate, PAP, and stroke volume (P < 0.05) occurred withexercise. In comparing rest and exercise 2, and PVR valuesdetermined by the model and independent methods, and incomparing each method for these values, there was no signifi-cant difference. Model-derived and independently derived es-timates of C, were significantly different at rest (P < 0.04) andexercise (P < 0.001). There was no significant difference be-tween rest and exercise values o f C, by either method. Themodel estimates of PVR at rest (64 t 11 dyne so cms5) andexercise (41 t 7 dyn . so cm-) (P = 0.06) and the model 2, valueat rest (22 k 3 dyne so cmW5) were appropriate. The model C,values at rest (0.22 t 0.05 ml.mmHg-lo kg-) correlated withpreviously reported normalized values in other species. Thisstudy reports the successful use of a parameter estimationprocedure based on the three-element windkessel model todescribe pulmonary artery compliance in normal humans.pulmonary characteristic impedance; modeling; windkesselmodel

DETAILED DESCRIPTIONS of the structure and functionof the circulatory system have been attempted since theearly part of the 18th century beginning with the effortsof Reverend Stephen Hales (5a). He emphasized thefunctional property of elasticity of the vascular tree andbelieved that the arterial system behaved as a large,distensible reservoir, later referred to as a windkesselin the German literature. Since that time, numerousmathematical models have been contrived to describeand evaluate the properties of pulsatile flow and pressurewithin the arterial system (2, 19, 20, 22, 24).One such mathematical approach has been to apply anelectrical analogue of a three-element windkessel modelto give estimates of characteristic impedance, vascularresistance, and compliance of the systemic arterial cir-culation (22). Recently, this model has been integrated

with a computer-processing algorithm to obtain the threeparameters of vascular function on a beat-to-beat basisand during transients from measured pressure and flowdata (20). To date, the application has generally beenlimited to the systemic arterial tree in the animal studies(7, 20) with one report in humans (6).Detailed studies on the pulmonary input impedancespectrum in humans have been limited to the restingstate (12) or in vitro electrical analog methods (15). Areliable method to determine pulmonary arterial compli-ance in humans has not been suggested. An accuratemeasurement of the arterial compliance may provideuseful information in the evaluation of pulmonary hy-pertension or in determining medical therapy for pul-monary hypertension. Furthermore, the contribution ofthese pulmonary arterial parameters, pulmonary arterialcompliance (C,), characteristic impedance (2,)) vascularresistance (PVR) at rest and during submaximal supineexercise, has not been investigated and might provideinsight into the basic pulmonary physiology. The presentstudy in normal humans was designed to evaluate theutility of a parameter estimation procedure based on thethree-element windkessel model applied to the pulmo-nary arterial circulation to describe the C,, Z,, and PVRat rest and during supine submaximal exercise.METHODS

Eight patients were studied during elective routinecardiac catheterization performed for various clinicalindications, the most common of which was a chest painsyndrome. Medicines were discontinued before study.There was no evidence of organic heart disease by hemo-dynamics at rest or during supine submaximal exerciseor as judged by left ventricular cineangiography or cor-onary arteriography. Therefore, all patients were consid-ered physiologically normal and without demonstrablecardiovascular pathology. All patients were studied in afasting basal state and were unsedated or very lightlysedated with diazepam (10 mg orally -1 h before theprocedure). All patients were studied with informed con-sent. This protocol was reviewed and approved by ourmedical center Institutional Review Board.Right and left heart cardiac catheterizations were per-formed using the Sones technique from a right brachialapproach. A balloon-tipped, flow-directed, thermodilu-tion catheter was advanced through the right heart

H1823


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H1824 PULMONARY ARTE RIAL CO MPLIANCE IN HUMANS

PULMONARY ARTERYEMF VELOCDTY PROBEPULMONARY ARTERYSENSORRIGHT VENTRICULARSENSORR1GHT ATRIALSENSOR

FI G. 1. Typicaleter catheter.

placeme nt of right heart multisen sor micromanom-

chambers in routine fashion, and the tip was positionedin the distal pulmonary artery. A second right-heartcatheter, which contained three solid-state pressure sen-sors and an electromagnetic flow velocity probe, was usedto record high-fidelity right heart hemodynamics. Thethree pressure sensors were mounted laterally with thedistal sensor, and the electromagnetic flow velocity probewas mounted at the same site (model no. SSD-192, MillarInstruments, Houston, TX). The distance between thetip of the catheter and the distal pressure sensor withthe electromagnetic flow probe was 9 cm. The distancebetween the distal and middle sensors was 5 cm; betweenmiddle and proximal sensors, there was a 12-cm distance.The catheter was manipula ted under fluoroscopic guid-ance so that the distal sensor and electromagnetic flowvelocity probe were positioned in the main pulmonaryartery just above the pulmonary valve, the middle sensorin the right ventricular outflow tract, and the proximalsensor in the right atrium (Fig. 1). Details of the technicalcharacteristics of these sensors, including frequency re-sponse, drift characteristics, and calibration techniques,have been previously described (8, 13).

During the rest and exercise studies, oxygen consump-tion was determined by collecting a 5-min Douglas bagand measuring oxygen content using mass spectrometry.Simultaneously with the gas collection, arteriovenousoxygen content difference was derived from hemoglobinoxygen saturation determinations from the brachial andpulmonary artery. Right heart oximetry was used todocument absence of a left-to-right shunt. Cardiac out-put was t/hen calcula ted using the direct Fick method.

Cardiac outputs were also measured using the thermaldilution technique averaging three or more output deter-minations. The bolus was 10 ml of dextrose water chi lledto 6C. The cardiac outputs by the two methods agreedwith 600 ml/m in difference, and the cardiac outputsquoted are those from the Fick method. When properpositioning of the catheters was achieved and a steadystate confirmed by stable heart rate and pulmonaryartery oxygen saturation determinations, simultaneouspulmonary artery flow and pressure, right ventricular,and right atr ia1 pressures were recorded.

After the hemodynamics were recorded at rest, pa-tients had their legs elevated and feet positioned on abicycle ergometer (Quinton Instruments, Seattle, WA).The average work load given for submaximal supineexercise was 2,000 ft lb* s-l ranging between 710 and3,250 ft. lb l s-l depending on the judgment of the attend-ing physician. Subjects were exercised a ful l 5 min aftera steady state was verified by a stable heart and pulmo-nary artery oxygen saturation determinat ion. Hemody-namics were recorded in similar fashion to the rest study.Finally, ventriculography and coronary cineangiographywere performed after rest, and exercise hemodynamicswere completed for verification of normality.

Data analysis. Data were orig inally recorded and savedon l-in. 14-channel FM analog tape (Honeywell model101). The cases were iden tified and a representativesteady-state portion of the rest and exercise data weredigitized at a 500-Hz sample rate using a MASSCOMP5500 mainframe computer (MASSCOMP, Westford,MA).Using a generic signal processing program (DaDispversion l.O5B, DSP, Cambridge, MA), four representa-tive beats at the end-expiratory phase of simultaneouspulmonary artery pressure and flow at rest and duringexercise were selected. The mean pulmonary capillarywedge pressure was subtracted from the indiv idual beatsfor both rest and exercise states. The pulmonary arterialflow velocity was calibrated to the Fick-derived strokevolume. Four representative beats were then averaged.The averaged simultaneous pressure and flow waveformswere used in a custom-programmed parameter identifi-cation algorithm based on the three-element windkesselmodel that has been previously described (7). The curve-fitt ing algorithms adjust the three parameters throughseveral iterations until the best fit (minimal of the chi-square) of the calcula ted flow to the measured flow hasbeen achieved (see Fig. 2). Independent calculations of

500 MW8.C Z 500 YLhocFI G. 2. Illustration of 3-element windkessel model

(middle) and example of fit to pulmonary artery flowPAF calcula ted by model at rest and exercise. Mid e: C,

compliance; R, resistance; Z,, characteristic impedance.Left and right: C, calcula ted; M, measured; PAF, pul-monary artery flow; PAP , pulmonary artery pressure.


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PULMONARY ARTE RIAL CO MPLIANCE IN HUMANS HE325TABLE 1. Summary of demographic and hemodynamicdata at rest and during supine submaximal exercise

Patient

AgeSexwtFt-lb/sHR

RE

coRE

SVRE

PASRE

PAdRE

PAmRE

LVesRE

LVedRE

AosRE

AodRE

AomRE

34 34 47 38 53 67 46 29M F M M F F M M82 85 79 83 95 75 99 107

3,200 710 1,640 2,170 1,200 1,200 2,250 3,25067 59 78 66 72 90 65 58108 82 108 114 90 122 91 140

6.5 4 8.6 7.2 7.2 8.1 4.2 8.518.8 6.9 15.2 15.5 10.5 10.3 9.7 19.497 69 110 109 99 90 65 146174 84 141 136 117 84 106 13918 20 19 19 22 16 25 2230 31 26 26 35 22 34 31

8 7 7 8 8 7 12 912 11 11 11 12 13 15 912 11 13 13 12 11 16 1824 18 20 19 23 13 24 12

112 122 110 116 148 100 119 118135 145 136 143 174 112 160 14310 10 6 12 6 9 7 1316 15 15 12 14 12 15 16

112 122 110 116 148 100 119 118135 145 136 142 174 112 160 143

75 7882 85

88 101105 111

7485

8895

72 76 70 74 7588 95 78 94 98

95 103 83 96 96127 125 89 122 118

the three parameters were also performed to allow com-parison of values determined by traditional methodologywith those estimated by the computer model. Calculationof characteristic impedance was performed by applyinga Fourier analysis to averaged pulmonary artery pressureand flow waveforms. Amplitude of moduli of pressureand flow harmonics were divided. The impedance mod-ulus between 3rd and 12th harmonic were then averagedto give characteristic impedance. Pulmonary vascularresistance was considered the 0th harmonic of the imped-ance modulus. The arterial compliance was estimated bydividing the right ventricular stroke volume by the pul-monary arterial pulse pressure (systolic minus diastolicpressure). For comparison with other species, complianceestimates were normalized by dividing by the body weightin kilograms. The paired t test was used to test for asignificant difference between calculated and modeledvalues of the three parameters and for the differencesbetween rest and exercise values of those parameters.Values of P < 0.05 were considered significant. All valuesare presented as the mean t SE.

RESULTSThe subject population consisted of five men and threewomen aged 40 t 3 yr. All subjects had normal hemo-dynamic parameters (Table 1) at rest and with supinesubmaximal exercise. The subjects had normal left ven-triculography and coronary angiography. The averageheart rate increased by 37 (P < 0.001) with exercise.

The mean cardiac output at rest was 6.5 l/min, whichincreased 50 (P c 0.005) with exercise with strokevolume increasing 20 (P < 0.03). The mean pulmonaryartery pressure increased 29 (P < 0.02) during exercise.Pulmonary root flow signals are broad at the base withslower ascending and descending segments. The diastolicpulmonary artery pressure decays at rest were slow,indicating longer time constants.Individual values of the three parameters derived fromthe windkessel model and the calculated method duringrest and exercise are shown in Table 2. The averagedparameters by the modeled and calculated methods atrest and with supine submaximal exercise are shown inTable 3. The relative error for each parameter estimationwas 0.90.The differences in characteristic impedance and vas-cular resistance at rest or during exercise using theestimations returned by the model and the independentlycalculated values were not statistically significant (seeFig. 3). There were also no significant differences be-tween rest and exercise characteristic impedance deter-minations by either method. Pulmonary vascular resist-ance, however, decreased by an average of 50 from restto exercise that did not quite meet significance (P =0.06). In contrast, there was a significant differencebetween arterial compliance values determined by themodel and those calculated (see Fig. 4). The modeledpulmonary arterial compliance at rest gave a mean valueof 19.9 -+ 5.4 ml/mmHg, which was 2.5 times greater (P< 0.05) than the arterial compliance (8.0 t 0.87 ml/mmHg) determined by independent estimation. Duringexercise, this difference increased to 3.4 times (P c 0.02)with the modeled arterial compliance giving a mean valueof 27.5 t 3.63 ml/mmHg and the independently calcu-lated arterial compliance estimating a mean of 8.12 t0.66 ml/mmHg. However, the difference from rest toexercise by either method was not statistically signifi-cant. The modeled arterial compliance did reveal a trend(P = 0.06) to increase from rest conditions by -30during exercise. When both modeled and independentlyderived arterial compliances were normalized for thesubjects weight in kilograms (Table 4), there was still asignificant difference between modeled and calculatedmethods at rest (P < 0.02) and with exercise (P c 0.003).However, there were no significant differences betweenthe rest and exercise values for each respective method.DISCUSSION

The present study evaluated the pulmonary arterialcompliance by a parameter estimation procedure basedon the three-element windkessel model, which addi-tionally determined the characteristic impedance and thevascular resistance, at rest and during supine submaxi-


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PULMONARY ARTE RIAL C OMPLIANCE IN HUMANS

REST EXERCISECONDITION OF STUD Y

TABLE 2. Modeled and calculated parameters at restand with supine submaximal exercisezz C PVR

Patient R E R E R E-- ~ _______ ~m c m c m c m c m C m c

15 15 23 43 19 10 34 10 50 58 21 3924 23 18 25 9 6 33 9 75 63 41 4024 19 12 16 9 6 32 9 75 86 32 3817 26 20 25 20 8 42 10 86 78 16 3038 28 16 19 34 7 13 5 25 64 75 8618 12 7 17 13 10 9 9 60 54 35 4522 25 17 29 5 5 14 6 119 148 40 5017 26 10 9 50 12 45 7 25 36 45 35

Z,, charac teristic impedan ce (dyn . s. cma5); C, comp liance (ml.mmHg- . kg-l); PVR, pulmonary vascular resistanc e (dyn +s. cmW5); R,rest; E, exercise; c, calculated; m, modeled.

ma1exercise in normal humans. We found model-derivedestimations of characteristic impedance and vascularresistance were similar to independent calculations ofthese variables at rest or during exercise. Furthermore,the variables of these three parameters were statisticallyunchanged with supine submaximal exercise despite asignificant change in the pulmonary artery pressure,stroke volume, and heart rate.The values at rest for Z,, both model derived andindependently calculated, are similar to reported valuesat rest in humans ranging from 20 to 23 dyn. s.cmB5 (9,

LEGENDlz izzlVR,MODELPVRwCALCZc-MODELZc-CALC

FI G. 3. Comparison of characteristicimpedan ce and pulmonary vascular re-sistance determined by model and cal-culated methods at rest and during ex-ercise (mean SE). There was no sig-nificant difference between modeled andcalcula ted values or between rest andexercise values (talc, calculated; PVR,pulmonary vascular resistanc e; Z,, char-acteristic impedance).

10, 15). Model-derived and calculated PVR at rest andwith exercise correlated with previously reported values(5). Previous mathematical models have been used topredict the pressure and flow of the pulmonary circula-tion (3, 14, 16, 23). Piene (15) used a four-element modeland validated this approach successfully in cats. Unlikeparameters of resistance, however, there is no easilyvalidated method for the determination of absolute pul-monary arterial compliance in vivo for humans. Limitedstudies on pulmonary arterial compliance have been per-formed in animals (12, 17). Milnor et al. (11) evaluatedpulmonary compliance at rest in patients with valvularheart disease and pulmonary hypertension. The totalpulmonary compliance was estimated by dividing thetotal pulmonary blood volume (determined by a dyedilution technique) by the mean intravascular pressurecalculated as the mean pulmonary artery pressure plusleft atria1 pressures divided by two. The averaged totalpulmonary compliance (arterial plus venous compliance)normalized to body weight was found to be 0.408 ml.mmHg- l kg-l in patients with normal PVR. Shoukas(17) found in dogs the mean total pulmonary vascularcompliance that included arterial and venous contribu-tions approximating 0.30 ml mmHg- . kg-, similar tothe results of Milnor in humans. Shoukas (17) furtherdemonstrated that the portion of total pulmonary vas-cular compliance attributed to the pulmonary arterialtree was 0.18 ml. mmHg-l . kg-, which closely approxi-mates 0.22 ml. mmHg- l kg- found in the present study.Utilizing a normalization of compliance values to body

TABLE 3. Averaged modeled and calculated parameters at rest and with supine submaximal exercise

R E RPVR C

E R EModeled 22t2.6 16t1.89 64t11.18 38t6.34 20t5.4 28t4.89Calculated 2222.0 23t3.64 73211.92 45t6.18 8-c-0.87* 8t0 .67-f

Z,, charac teristic impedan ce (dyn . so cmm5); PVR , pulmonary vascular resistan ce (dyne s m mM5); C, pulmonary arterial comp liance (ml. mmHg- *kg-l); R , rest; E, exercise. * Calculate d comp liance at rest was significa ntly different (P = 0.04) from modeled comp liance. t Calcula ted comp liancewith exercise w as significa ntly different (P < 0.003) from modeled comp liance.


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PULMONARY ARTE RIAL COMPLIANCE IN HUMANS HI827LEGEND

EXERCISEOF STUDY

TABLE 4. Normalized compliancesPatient Rest Exercisem C m C

Eza COMPLIANCFMODELCOMPLIANCLCALC

FI G. 4. Compa rison of pulmonary ar-terial compliance determined by modeland calculated methods at rest and withexercise (mean t SE). When comparingmodeled and calculated arterial compli-ance, there was a significant differenceat rest and with exercise (*P < 0.05).There was, however, no signif icant dif-ference between rest and exercise byeither method (talc, calculated ).

1 0.23 0.12 0.42 0.122 0.11 0.07 0.39 0.113 0.11 0.07 0.38 0.114 0.24 0.01 0.5 0.125 0.36 0.07 0.14 0.056 0.17 0.13 0.12 0.127 0.05 0.05 0.14 0.068 0.46 0.11 0.42 0.06

Mean 0.22t0.05 0.08t0.01* 0.30t0.05 0.09+0.01 j-Normalized comp liances (ml. mmHg- l kg-) during exercise by

modeled and calculated methods. c, calculated; m, modeled; * Meancalculated compliance was significantly different (P < 0.02) from meanmodeled compliance. t Mean calculated compliance was significantlydifferent (P < 0.003) from mean modeled comp liance with exercise.

weight or surface area allows for the comparison ofresults between species. When the modeled and calcu-lated C, were normalized to body weight and comparedwith the pulmonary arterial compliances obtained byShoukas (17), then the modeled C, appeared a morereasonable estimate of the arterial compliance than thatapproximated by the independently derived method. Be-cause the independently derived method provides only acrude estimate of compliance that dynamically changesthroughout the cardiac cycle, a discrepancy betweenmethods was expected. The trend seen in the pulmonaryartery compliance may have been influenced by an in-crease in the cross-sectional area of the distal pulmonaryarteriolar bed. Thus the trend toward an increase inarterial compliance may have been determined more bya peripheral phenomenon rather than one involving themain pulmonary artery and major branches.Our findings and hypothesis are further supported byYu et al. (25), who noted significant increases in pul-monary blood flow in humans during submaximal supine

exercise with minimal changes in pressure. In addition,it has been shown that the pulmonary capillary bloodvolume increases in exercise secondary to opening ofparallel channels (4, 21). These changes would cause anincrease in the compliance peripherally. The resultantincrease in the arteriolar cross-sectional area probablyalso explains the trend (P = 0.06) toward a decrease inthe PVR. Theoretically, this trend may occur becausethere is redistribution of the vascular volume when su-pine causing an increase in the arteriolar cross-sectionalarea. Thus the change is not as great as expected withupright exercise (5).There are several limitations to the present study.Patients in this study received an elective cardiac cath-eterization because of atypical chest pain syndromes.Therefore, these patients may not necessarily representnormal patients hemodynamics at rest or with exercise.Also, because the parameter estimation procedure isbased on the three-element windkessel model, it does notanalyze the reflected waves that may represent a majorportion of the pressure and flow waveform of the pul-monary system, and one might anticipate erroneous es-timations of the parameters. However, given the excel-lent correlation of all three parameters with previouslyreported values at rest, and given the high correlationcoefficients and low relative errors by the model, themodel does describe the circulatory dynamics appropri-ately. It is possible, however, that the pulmonary circu-lation may be better defined by a distributed circulatorymodel (I) that attempts to compensate for the reflectionsin the analysis. Another limitation is that no previousstudy has analyzed these parameters during exercise;therefore, the explanation of the physiological mecha-nism during exercise is hypothetical.This study is one of the most extensive evaluations todate of pulmonary vascular dynamics at rest and withexercise in a patient population without overt organicheart disease. This study also demonstrated the success-


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Hl828 PULMONARY ARTERIALful use of a parameter estimat ion procedure based on thethree-element windkessel model to model pulmonarycirculatory dynamics in humans. This approach, al-though invasive, is possibly the simplest and most accu-rate method currently available for the evaluation of thearterial compliance of the pulmonary circulatory systemin vivo. In humans, this model is capable of describingthe pulmonary vasculature system more completely thanpreviously and may prove to be beneficia l in the evalua-tion of pulmonary hypertension (reactive vs. fixed hy-pertension) as well as perhaps def ining a better thera-peut ic approach to patients with pulmonary hyperten-sion. Studies are ongoing to test the applicability of adistributed model to the pulmonary vascular tree and toevaluate subjects with pulmonary hypertension.

We are grateful for the graphics work by Roberto Rios of theDepartment of Clin ical Investigation, and we appreciate the editorialassis tanc e of Margaret Latham in preparation of the manus cript.

Th is work wa s supported in part by a grant from North Amer icanTreaty Organization Scie ntific Affairs Division RG 86/006, N. Wester-hof and R. D. Latham.

The views expressed herein are the private views of the authors andare not to be construed as offic ial or representing those of the Depart-ment of the Army or the Department of Defense.

Addres s for reprint requests: D. M. Slife, Cardiology Service, BeachPavilion , Brooke Army Medical Center, Fort Sam Houston, TX 78234-6200.Received 9 June 1989; accepte d in final form 16 January 1990.REFERENCES

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COMPLIANCE IN HUMANS

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1990 - Slife - Pulmonary Arterial Compliance at Rest and Exercise in Normal Humans