respiratory-induced variability of pulmonary arterial pressure measurements in cattle

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Page 1: Respiratory-induced variability of pulmonary arterial pressure measurements in cattle

Veterinary Research Communications, 14 (1990) 227-233 Copyright 8 Rluwer Academic Publishers bv - Printed in the Netherlands

RESPIRATORY-INDUCED VARIABILITY OF PULMONARY ARTERIAL PRESSURE MEASUREMENTS IN CAlTLE

H. AMORY, T. ART, D. DESMECHT, F. ROLLIN AND P. LEKEUX Laboratory for Functional Investigation, Faculty of Veterinary Medicine, University of Liege, Belgium Correspondence address: Dr H. Amory, Service de Physiologie, Facultt de MCdecine VCtCrinaire (Cureghem), Universite de Liege, 45 rue des VCttrinaires, B-1070 Bruxelles, Belgium

Amory, H., Art, T., Desmecht, D., Rollin, F. and Lekeux, P., HEJO. Respiratory-induced variability of pulmonary arterial pressure measurements in cattle. Veterinary Research Communications, 14 (J), 227-233

The purpose of this study was to investigate the variability of the peak systolic (PAPS) and the end diastolic (PAPd) pulmonary arterial pressures induced by intrapleural pressure changes in cattle.

The pleural pressure (Ppl), the electrocardiogram and the pulmonary arterial pressure (PAP) were simultaneously recorded in five healthy calves under three different conditions, i.e. normoxia (N), normoxia with an added airflow resistance (R) and hypoxia (H). PAPS, PAPd and their corresponding transmural pressures were measured and averaged over 10 successive regular cardiac cycles. The maximum Ppl changes (maxAPp1) were measured on the same tracings. The variance and coefficients of variation were calculated for each set of vascular measurements.

MaxAPpl was significantly increased with mgard to N values during R and H conditions. This increase in maxAPp1 induced a simultaneous rise in the variability of PAP measurements, while in each condition, this variability was greatly lowered by use of the corresponding transmural pressure.

It was concluded that, in calves with high mawhPp1, the influence of respiration on PAP becomes considerable. In such cases, the use of transmural pressures rather than luminal pressures can greatly reduce the variability of these pulmonary pressure measurements and therefore increase their sensitivity.

Keywork cattle, pulmonary arterial pressure, respiration

INTRODUCTION

It has been shown that respiratory-induced fluctuations (RIF) in pleural pressure affect the intrathoracic vessels, causing a variation in the recorded luminal vascular pressure synchronized with these RIF (Hamilton et al., 1944). During inspiration, the pressure in the chest decreases, inducing a simultaneous fall in the pulmonary vessels’ hrminal pressure. In the same way, the rise in the chest pressure during expiration causes a simultaneous increase in the luminal pressure of the thoracic vessels (Hamilton et al., 1944).

Under physiological conditions, the changes in the pleural pressure are small and consequently the RIF of the puhnonary blood pressure are also small. On the other hand, when the variations in the pleural pressure are considerable, the influence of breathing on the pressure in the intrathoracic vessels becomes more marked (Rodbard ef al., 1956, Goetz and Manohar, 1986).

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It has been previously noticed that the pleural pressure changes in the bovine species become large under certain circumstances, such as in cattle suffering from respiratory disorders (Lekeux et al., 1985a,b,c) or exposed to an acute hypoxia (Rollin et al., 1989). In these situations pulmonary blood pressures probably undergo important RIF.

The purposes of this study were (1) to quantify the variability of peak systolic (PAPS) and end diastolic (PAPd) pulmonary arterial pressures induced by pleural pressure changes in calves in two different experimental conditions, i.e. increased airflow resistance and acute hypoxia and (2) to analyse the efficiency of using transmural instead of luminal pressures to reduce this respiratory-related pulmonary arterial pressure variability in cattle.

MATERIALS AND METHODS

Animals

Five healthy male calves (weight 54.2 f 2.9 kg; age 34 + 5 days) were used. Three of them were of the Friesian breed and the other two were of the Belgian White and Blue breed.

Measurement techniques

Pleural pressure (Ppl) was measured by means of an oesophageal balloon catheter coupled to a pressure transducer and an amplifier (Gould, Bilthoven, The Netherlands). The tip of the oesophageal catheter was positioned in the thoracic portion of the oesophagus between the crossing point with the aorta and the caudal media&ml lymph nodes. This position was standardized by use of the formula: Lcat (cm) = 0.65 + O.ll5BW (kg), where Lcut = distance between the nares and the oesophageal catheter tip and BW = body weight (Lekeux et al., 1984a).

Arterial pulmonary pressure (PAP) was obtained using a fluid-filled catheter (Swan-Ganz 7F, Gould) connected to an extravascular pressure transducer (Statham, Gould) and an amplifier (Sirecust, Siemens, Brussels, Belgium). The position of the vascular pressure transducer was standardized at the level of the shoulder joint. The Swan-Ganz catheter was brought to its pulmonary arterial position via an introducer (Desilet 8 F, Vygon, Brussels, Belgium) placed in the right jugular vein.

An electrocardiogram (ECG) was obtained by means of a telemetric system (Danika Electronics, Copenhagen, Denmark) as previously described (Lekeux et al., 1982).

All the parameters (Ppl, PAP and ECG) were simultaneously recorded on a rapid writing polygraph (ES 1000, Gould). Both pressure transducers were calibrated before and after each experiment with a water manometer.

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Protocol

During the experiment the calves were kept in a woodea stanchion in a normal standing position and no tranquillizers or general anaesthetics were used. The introducer was placed and fmed in the jugular vein and the animals were then givea one hour’s recuperation. After this they were equipped with the telemetric system, the oesophageal balloon catheter and a tight-fitting face mask (Lekeux et al., 1%). The Swan-Ganz catheter was advanced into the pulmonary artery. The position of the distal end of the catheter was controlled by continuous monitoring of the pressure curve. Pleural pressure, PAP and ECG were recorded in quiet resting animals (aormoxic without added airflow resistance valves).

After these measurements, a non-rebreathiag valve (Hans Rudolph, model 7200) was placed on the face mask. This produced an increase in airflow resistance. After 3 minutes, the same parameters were again recorded (aormoxic with added airflow resistance valves). Lastly, the non-rebreathing valve was connected via a Iway stopcock to a 135 L meteorological balloon filled with a hypoxic gas mixture (10% oxygen in nitrogen) for 3 minutes. At the end of this period, the parameters were recorded for the last time (hypoxic with added airflow resistance valves).

Calculations and statistical analysis

The peak systolic and end diastolic pulmonary arterial pressures were measured for 10 successive regular cardiac cycles. The simultaneous Ppl was measured for each of the PAPS and PAPd values. Peak systolic (TMPs) and end diastolic (TMPd) transmural pressures were obtained by subtracting each value of Ppl from its corresponding PAPS and PAPd respectively. The mean, the variance and the coefficient of variation were calculated for each set of 10 measurements.

The maximum Ppl changes (maxAPp1) were calculated by subtracting the minimum Ppl from the maximum Ppl for five successive regular respiratory cycles and averaging.

The calculations were performed for each of the three experimental conditions. Results are givea as mean f SEM for the live calves. The aormoxic with an added airflow resistance values and the hypoxic values were compared with the aormoxic without an added airflow resistance values by means of a paired t-test.

RESULTS

The calves responded to the added airflow resistance by a significant increase in maxAPp1. Breathing a hypoxic gas mixture through the same respiratory resistance caused a significant increase in maxAPpl, PAPS and TMPs (Table I).

The coefficients of variation and variances of the haemodynamic measurements are given in Table I and Figure 1 respectively. The variability of the PAP measurements increased with increasing maxAPpl, but was greatly reduced when PAP were expressed as traasmural instead of lumiaal pressures.

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Variance (mm Hg2)

a

120 1

1 100

SO i

60 1

n PAPS

El TMPs

Variance (mm Hg2)

N R H

Figure 1. Variance of pulmonary arterial peak systolic (a) and end diastolic (b) luminal and transmural pressures in three experimental conditions in calves (mean k SEM,n = 5). N = normoxia without an added airflow resistance; R = normoxia with an added airflow resistance; H = hypoxia with an added airflow resistance; PAPS and PAPd = peak systolic and end diastolic pulmonary arterial luminal pressure respectively; TMPs and TMPd = peak systolic and end diastolic pulmonary arterial transmural pressure respectively

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TABLE I The absolute mean values and coefficients of variation of puhnonary arterial pressure measurements and the absolute values of maximum changes in pleural pressure during three different experimental conditions in five healthy calves (mean f SEM)

Absolute mean values Coefficients of variation (mmHg) Pm

PAPS N R H

TMPS N R H

PAPd N R H

TMPd N R H

maxAPp1 N R H

37.0 + 3.3 43.7 f 2.3 63.0 + 4.6*

41.0 f 3.7 47.4 + 2.6 67.6 + 5.5*

15.6 + 2.7 15.2 + 1.4 23.9 k 3.8

19.2 + 3.0 22.9 f 2.1 27.6 + 6.3

5.4 f 0.5 10.8 + 0.6** 16.7 + 1.6**

9.4 2 3.3 13.9 + 1.1 16.1 + 0.6

5.3 + 1.1 8.1 + 1.2 7.5 f 0.2

21.5 + 6.0 22.2 f 6.6 23.5 f 4.2

8.1 + 1.6 10.3 + 3.2 10.0 r: 4.3

* Signiticantly different from N values, paired I-test,p G 0.05 **p G 0.01 PAPS = Peak systolic pulmonary arterial pressure TMPs = Peak systolic pulmonary arterial transmural pressure PAPd = End diastolic pulmonary arterial pressure TMPd = End diastolic pulmonary arterial transmural pressure maxAPp1 = Maximum pleural pressure change

DISCUSSION

Under normal conditions (normoxic without an added airflow resistance), the maxAPp1 was smah and within the physiological range (Lekeux et al., 19t34c) and the variability of the PAP measurements was low. When maxAPp1 reached values greater than those previously reported for healthy resting calves, with an added airflow resistance or during hypoxia, the variability of the PAP measurements was high. This suggests that, in cattle with large Ppl changes, the high variability of PAPS and PAPd

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measurements may be a source of inaccuracy or error and, consequently, of loss of sensitivity of the technique.

The opportunity to reduce this variability by the use of transmural pressures instead of huninal pressure was investigated. In each experimental condition, PAP measurement variability was greatly reduced by use of the corresponding transmural pressures, as shown by the considerable lowering of the variance and coefficient of variation (Table I and Figure 1). The conversion of pulmonary luminal pressures to pulmonary transmural pressures (TMP) is therefore a valuable way of reducing the variability of PAPS or PAPd measurements.

In this study, Ppl was measured indirectly by means of the oesophageal balloon technique. Ppl obtained in this way do not exactly reflect the pressure surrounding the pulmonary artery at the precise level of the intravascular pressure measurement (Fishman, 1985). Therefore, the calculated transmural pressures represented only an approximation to the real TMP. However, this lack of precision must be small because the vertical gradient of Ppl in the bovine thorax has been shown to be low (Lekeux er al., 1984b).

In most pulmonary and haemodynamic studies, mainly because of technical limitations, the PAP are expressed as luminal pressures. It would be very interesting to perfect a technique to measure TMP directly. One advantage of this approach would be the possible reduction of the influence of pleural pressure changes on the variability of pulmonary wedge pressure recordings. Indeed, when maxAPp1 are important, as during muscular e?ercise (Goetz and Manohar, 1986) or in animals suffering from respiratory disorders (Kung et al., 1978), the respiratory artefacts on a pulmonary wedge pressure tracing are so marked that it becomes difficult to read and to interpret.

It was concluded that, in calves with high maxAPpl, the influence of respiration on PAPS and PAPd is considerable. In such cases, the use of transmural pressures rather than luminal pressures can greatly reduce the variability of the PAP measurements and therefore increase their sensitivity.

ACKNOWLEDGEMENTS

The authors are very grateful to J.C. Leroy, M. Leblond and J.F. Deneubourg for their technical assistance. This work was supported by I.R.S.U., convention no. 513L4. H. Amory is a Research Assistant supported by a contract with the National Fund for Scientific Research (Belgium)

REFERENCES

Fishman, A.P., 1985. Pulmonary circulation. In: A.P. Fiihman and A.B. Fisher (eds.), Handbook of Physiology, Section 3. Respiration, Vol. 1, (American Physiological Society, Bethesda, Maryland), 93-166

Goetz, TX. and Manohar, M., 1986. Pressures in the right side of heart and esophagus (pleura) in ponies during exercise before and after furosemide administration. American Journal of Veterina?y Reseamh, 47(2),270-276

Hamilton, W.F., Woodbury, R.A. and Harper, H.T., 1944. Arterial, cerebrospinal and venous pressures in man during cough and strain. American Journal of Physiology, 141,42-45

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Kung, M., Reinhart, M.E. and Wanner, A., 1978. Pulmonary hemodynamic effects of lung inflation and graded hypoxia in conscious sheep. Journal of Applied Physiology, 45,949-956

Lekeux, P., Henroteaux, M. and Bienfet, V., 1982. Comparison du type et de la fr6quence relative des principales arythmies cardiaques obsen&s chex Ies chevaux en fonction de leuts performances en course: une ttude radiotelem&rique. Annaks de Mkdecine V&rinaire, W, 205-208

Lekeux, P., Hajer, R and Breukink, HJ., 1984a. Intmthoracic pressure measurement in cattle: standardized procedure. Gznudian Journal of Comparative Medicine, 45,420-421

Lekeux, P., Hajer, R and Breukink, HJ., 1984b. Pulmonary function testing in cahw technical data. American Journal of Veterinary Research, 45,342-345

Lekeux, P., Hajer, R and Breukink, HJ., 1984c. Effect of somatic growth on pulmonary function values in healthy Friesian cattle. American Journal of Veterinary Research, 45,2003-2007

Lekeux, P. Hajer, R and Breukink, HJ., 1985a. Physiological effects of experimental verminous bronchitis in Friesian caIves. Canadian Journal of Comparative Medicine, 49,205-207

Lekeux, P., Hajer, R and Breukink, HJ., 1985b. Longitudinal study of the effects of hmgwom infection on the bovine pulmonary function. American Journal of Veterimq Research, 46,1392-1395

Lekeux, P., Hajer, R, Van Den Ingh, T.S.GA.M. and Breukink, HJ., 198%. Pathophysiological study of Imethyiindole-induced pulmonary toxicosis in immature cattle. American Journal of Veterinaty Research, 46,1629-1631

Rodbard, S., Kari, V. and Heiman, D.P., 1956. The diagnostic significance of the respiratory fluctuations of the pulmonary arterial pressure in man. American Heart Journal, 52,182-192

Rollin, R, Amory, H., Desmecht, D., Linden, A., Art, T. and Lekeux, P., 1989. Effect of acute hypoxia on the bovine ventilatoty mechanics. Archives Intemationales de Physio&ie et de Biochimie, !?7,86

(Accepted: 19 Januaty 1990)