Impedance Cardiography Versus Echocardiography

ORIGINAL ARTICLE Noninvasive cardiac monitoring in pregnancy: impedance cardiography versus echocardiography

J Burlingame1, P Ohana2, M Aaronoff1 and T Seto3

OBJECTIVE: The objective of this study was to report thoracic impedance cardiography (ICG) measurements and compare them with echocardiography (echo) measurements throughout pregnancy and in varied maternal positions. METHOD: A prospective cohort study involving 28 healthy parturients was performed using ICG and echo at three time points and in two maternal positions. Pearson’s correlations, Bland–Altman plots and paired t-tests were used for statistical analysis. RESULT: Significant agreements between many but not all ICG and echo contractility, flow and resistance measurements were demonstrated. Differences in stroke volume (SV) due to maternal position were also detected by ICG in the antepartum (AP) period. Significant trends were observed by ICG for cardiac output and thoracic fluid content (TFC; Po0.025) with advancing pregnancy stages. CONCLUSION: ICG and echo demonstrate significant correlations in some but not all measurements of cardiac function. ICG has the ability to detect small changes in SV associated with maternal position change. ICG measurements reflected maximal cardiac contractility in the a AP period yet reflected a decrease in contractility and an increase in TFC in the postpartum period.

Journal of Perinatology (2013) 33, 675–680; doi:10.1038/jp.2013.35; published online 16 May 2013 Keywords: thoracic impedance cardiography; echocardiography; pregnancy; labor

INTRODUCTION changes in thoracic electrical impedance during the cardiac cycle Cardiac disease has become one of the most common causes of and produce hemodynamic parameters that are highly producible pregnancy-related mortality and a potentially preventable cause and strongly correlate with invasive measures such as thermo- 16–18 of mortality.1–5 With the increasing impact of cardiac disease on dilution in the non-pregnant state. maternal mortality, noninvasive, portable and less labor-intensive ICG directly measures parameters of left ventricular contractility, cardiovascular monitoring might improve maternal outcomes. including the left ventricular ejection time (LVET), velocity index Women undergo significant structural and cardiovascular changes (VI), pre-ejection period (PEP) and directly measures SV, a during pregnancy that put them at risk for increased morbidities measurement of flow, using the Z MARC algorithm. Indirect, or due to pre-existing or new onset of cardiac disease. These changes derived, measures of systolic function include the systolic time have traditionally been documented using invasive monitoring ratio (STR) defined as the PEP or electrical systole divided by the (indirect Fick method and dye dilution indicator) and labor- LVET or mechanical systole, and acceleration index (ACI).19 intensive echocardiography (echo) with and without doppler.6–12 Calculations of systemic vascular resistance rely on estimates of During pregnancy, cardiac function also changes with position. the central venous pressure, which are potentially less reliable in Cardiac output (CO) increases with uterine displacement in the left the pregnant patient. Other assumptions made when using ICG lateral recumbent position, as increased venous return occurs with include that there are no valvular defects and no respiratory decompression of the great vessels.13,14 diseases.20 Currently echo is the most commonly used assessment of ICG has been proposed as an alternative method for monitoring cardiac function in pregnant woman. With echo, left ventricular cardiac function that is easy to use, cost-effective, reproducible function and contractility can be measured by way of the ejection and less operator and interpreter dependent than echo.21 ICG, fraction (EF), left ventricle end-diastolic diameter, fractional unlike echo, has the ability to directly assess cardiac contractility, shortening (FS) and mean velocity of circumferential fiber SV and to measure thoracic fluid content (TFC). Although there shortening.15 Echo has its limitations in the assessment of may be instances in which echo and ICG may substitute for one contractility, for example, the assessment of left ventricular EF another in the care of a pregnant woman, it is more likely that that has significant inter- and intra-observer variability and subtle these fundamentally different cardiac monitoring technologies changes in FS and EF may not be detected. Whereas echo will complement one another. measures heart function using changes in heart structure and This study describes and compares ICG and echo measures flow, impedance cardiography (ICG) directly measures electrical of contractility, flow and resistance. ICG and echo measurements impedance and thereby contractility and stroke volume (SV). were obtained at three different time points during pregnancy, and ICG is easily obtained using four electrode sensors placed on ICG measurements were obtained in two physiologically different the patient’s neck and thorax, ICG measurements are based on maternal positions. We hypothesize that ICG measurements of

1Department of Obstetrics, Gynecology and Women’s Health, John A. Burns School of Medicine, The University of Hawaii, Honolulu, HI, USA; 2The Research Corporation of the University of Hawaii, Honolulu, HI, USA and 3The Queen’s Medical Center, Center for Outcomes Research and Evaluation, Honolulu, HI, USA. Correspondence: Dr JM Burlingame, Department of Obstetrics, Gynecology and Women’s Health, John A. Burns School of Medicine, University of Hawaii, 1319 Punahou Street, Suite 824, Honolulu, HI 96826, USA. E-mail: [email protected] Received 17 August 2012; revised 16 January 2013; accepted 12 February 2013; published online 16 May 2013 Impedance cardiography versus echocardiography J Burlingame et al 676 contractility, flow and resistance will correlate with similar echo RESULTS measurements and will also be able to detect anticipated changes We enrolled 28 parturients (age 30.8±5.2 years, BMI 30.6± in maternal physiology with changes in maternal position and 6.3 kg m À 2, 34.0±1.2 weeks gestation, gestational age at delivery stages of pregnancy. 38.8±1.2 weeks), with 35.7% (n ¼ 10) of subjects pregnant for the first time. A total of 64 ICG and echo paired measurements were carried out: 26 AP and 18 IP during different stages of labor and 20 METHODS PP. Thirteen participants were evaluated at all the three time Before initiating this prospective cohort study, IRB approval was obtained points. Ten of the 28 participants delivered by cesarean section. and all study participants were consented before enrollment. Recruitment When comparing the same flow and resistance parameters (CO, took place at the Queen’s Medical Center and Kapiolani Medical Center for SV and SVR) between ICG and echo, Pearson’s correlations were Women and Children in Honolulu, Hawaii, between April 2009 and April 2010. Inclusion criteria included women 18–45 years with an uncompli- statistically significant in the LLRSP for SV and SVR AP; SV, CO and cated pregnancy and gestational age of at least 32 weeks. Exclusion criteria SVR IP; and SVR PP; and in the SR60P for SV and SVR AP; and SVR included any pre-existing heart disease, diagnosed hypertension or PP. Means with s.d.s and correlation coefficients for both echo and pulmonary edema, height o48 inches or 490 inches, weight o67 lbs or ICG are described in Table 1. 4341 lbs and multiple gestations. The comparison of the ICG measurements between the two The three time points for data collection were antepartum (AP) with a positions did not show any consistent differences. Other than minimum of 32 weeks gestation, intrapartum (IP) and postpartum (PP) changes detected in AP SV, there was little effect of maternal within 48 hours of delivery. To be included in analysis, each participant position on ICG readings as described in Table 2. Individual partici- had to have at least two of the three visits completed. ICG values were pant’s changes in SV during the AP period are shown in Figure 1. recorded twice consecutively, once in the left lateral recumbent supine position (LLRSP) and once in a semi-recumbent position at an angle of While correlations measure the data’s linearity, Bland–Altman about 601 position (SR60P). Echo values were only recorded in the LLRSP plots show the data’s agreement using mean differences immediately before or after the ICG measurements using the SonoSite (how much higher or lower one measure is than the other) and CardioDynamics BioZ Dx device (Bothell, WA, USA) (ICG). Blood pressure confidence intervals (what is the variability of the differences and was measured separately for each ICG reading. An estimated standard is it small enough to warrant the use of one device in place of the central venous pressure of 6 mm Hg was used. other). When comparing measurements made by ICG and echo, A certified cardiac sonographer using a General Electric Vivid e (echo; Bland–Altman plots showed acceptable (at least 95%) but modest General Electric, Waukesha, WI, USA) with images obtained in the LLRSP, agreement between ICG contractility parameters (STR, LVET, PEP, performed transthoracic echo exams. Standard 2-dimensional images and VI and ACI) and echo contractility parameters (EF and FS) most Doppler parameters were obtained from the parasternal and apical windows according to standard methods.22 Left ventricular end-systolic consistently during the AP period (Table 3). Bland–Altman plots and end-diastolic chamber dimensions were obtained from M-mode also showed acceptable agreement for both SV, CO and SVR in the images in the parasternal long-axis view, with 2-dimensional images used AP and IP periods and for SVR in the PP period (Table 4). if necessary. FS was calculated by dividing the change in left ventricular ICG demonstrated statistically significant different measure- chamber size from diastole to systole divided by the left ventricular end- ments across and between the different stages of pregnancy diastolic chamber size. EF was assessed by visual estimate by a single using analysis of variance with both multiple comparisons using a physician board-certified and Level III-trained in adult echo. CO was Bonferoni’s adjustment and with pairwise comparisons (Table 5). estimated using the velocity time integral of flow through the LV outflow CO and TFC demonstrated statistically significantly different tract multiplied by the area of the outflow tract based on measured physiology at all the three stages (AP, IP and PP) of pregnancy diameter.22 Both ICG and echo measurements were performed within 30 min of each other. (Figure 2). We used Pearson’s correlations to compare ICG and echo measurements of flow and resistance parameters (CO, SV and SVR (systemic vascular resistance)). Bland–Altman plots were used to study the agreement DISCUSSION between ICG (STR, LVET, PEP, VI and ACI) and echo (EF and FS) measurements of contractility. Paired t-tests were used to compare ICG ICG has already been validated as a reliable and convenient measurements in two different maternal positions. All analyses were modality for the evaluation of heart function in the non-pregnant 23–25 performed using IBM SPSS Statistics (version 19.0.1, Armonk, NY, USA). patient using invasive techniques and echo. However, our Continuous data are reported as means with s.d.s. study fills in some gaps left by previous observations of ICG use in

Table 1. Means and s.d.s for echo and ICG parameters at three stages of pregnancy in the left lateral recumbent supine position with Pearson’s correlations (r) and P-values

Time period Antepartum (n ¼ 26) Intrapartum (n ¼ 18) Postpartum (n ¼ 20)

Parameter Echo ICG Echo ICG Echo ICG

Stroke volume (ml) 74±21 84± 24 78±23 81±24 76±19 67±22 r ¼ 900.44 (P ¼ 0.023)* r ¼ 0.77 (P ¼ 0.000)** r ¼ 0.19 (P ¼ 0.423) Cardiac output (l min À 1) 5.8±1.6 6.4±1.9 5.6±1.3 5.8±1.5 5.6±1.1 5.0±1.6 r ¼ 0.25 (P ¼ 0.223) r ¼ 0.71 (P ¼ 0.001)** r ¼ 0.23 (P ¼ 0.329) Systemic vascular resistance (dynes s cm À 5) 993±392 921±319 1116±242 1093±314 1079±184 1324±473 r ¼ 0.56 (P ¼ 0.004)** r ¼ 0.66 (P ¼ 0.003)** r ¼ 0.34 (P ¼ 0.146) Acceleration index (per 100 s2) 100±38 109±23 101±30 Velocity index (per 1000 s) 63±18 65±11 58±14 Systolic time ratio 0.25±0.03 0.25±0.05 0.32±0.12 Pre-ejection period (ms) 76±874±683±16 Left ventricular ejection time (ms) 303±23 292±42 266±61 Abbreviations: echo, echocardiography; ICG, impedance cardiography. *P o0.05; **Po0.005.

Journal of Perinatology (2013), 675 – 680 & 2013 Nature America, Inc. Impedance cardiography versus echocardiography J Burlingame et al 677 Table 2. Effect of position on ICG measurements with paired t-test mean differences±s.d.s and (95% conﬁdence intervals)

Pregnancy stage Antepartum (n ¼ 26) Intrapartum (n ¼ 18) Postpartum (n ¼ 20)

Parameter 601 Seated Left lateral 601 Seated Left lateral 601 Seated Left lateral

Stroke volume (ml) 78±20 84±24 76±24 81±24 70±29 67±22 5.42±12.71 (.29, 10.56)* 4.83±22.94 ( À 6.57, 16.24) À 2.70±21.14 ( À 12.13, 6.73) Cardiac output (l min À 1) 6.1±1.5 6.4±1.9 5.7±1.6 5.8±1.5 5.1±2.0 5.0±1.6 0.28±0.80 ( À 0.43, 0.60) 0.14±1.69 ( À 7.0, 0.98) À 0.13± ( À 0.73, 0.48) Systemic vascular resistance 1050±313 921±319 1198±478 1,093±314 1430±617 1,324±473 (dynes s cm À 5) À 130.00±123.53 ( À 180.99, À 79.01)** À 105.33±442.53 ( À 325.40, 114.73) À 105.70±491.53 ( À 335.74, 124.34) Acceleration index 101±31 100±38 101±27 109±23 103±34 101±30 2 (per 100 s ) À 1.15±21.28 ( À 9.75, 7.44) 8.22±20.29 ( À 1.87, 18.31) À 1.55±23.62 ( À 12.44, 9.34) Velocity index (per 1000 s) 61±14 63±18 64±11 65±11 61±20 58±14 1.69±8.41 ( À 1.70, 5.09) 1.06±8.63 ( À 3.24, 5.35) À 3.15±11.34 ( À 8.46, 2.16) Systolic time ratio 0.26±0.06 0.25±0.03 0.27±0.06 0.25±0.05 0.30±0.06 0.32±0.12 À 0.01±0.07 ( À 0.04, 0.01) À 0.02±0.07 (0.02, À 0.06) 0.03±0.13 ( À 0.03, 0.09) Pre-ejection period (ms) 76±11 76±875±674±677±11 83±16 0.00±13.49 ( À 5.45, 5.45) À 1.22±7.70 ( À 5.10, 2.61) 6.00±13.73 ( À 0.42, 12.42) Left ventricular ejection 292±31 303±23 278±48 292±42 264±56 266±61 time (ms) 11.92±30.14 ( À 0.25, 24.10) 14.17±59.94 ( À 15.64, 43.97) 1.25±59.84 ( À 26.76, 29.26) Thoracic ﬂuid content 32.2±3.6 32.6±3.9 35.9±4.1 37.0±3.9 38.7±4.6 39.4±4.7 1 (k ohm À ) 0.40±2.14 ( À 0.46, 1.26) 1.16±1.24 (0.29, 0.54)** 0.66±1.43 ( À 0.01, 1.32) Abbreviation: ICG, impedance cardiography. *Po0.05; **Po0.005.

180 our ICG and echo data as they pertain to ﬂow (SV and CO) and 160 resistance (SVR) before, during and after labor also yielded 140 a number of statistically signiﬁcant correlations as well as Left Lateral acceptable agreement between these two methods of measuring 120 (mean = 84 mL hemodynamic data. 100 +/- 24) Interestingly ICG was able to detect a subtle increase in SV with 80 60 Degree Seated

SV (mL) change in maternal position in the AP period. This is possibly due (mean = 78 mL 60 to the increased venous return in the LLSRP. However STR, PEP +/- 20) 40 and LVET demonstrated no change in contractility with position change. This could be explained by the increasing blood volume 20 in the third trimester and increasing preload with SV increasing 0 0 5 10 15 20 25 30 according to the Frank Starling phenomena. The increased volume Antepartum Particpants (n = 26) should stretch the myocardium and increase contractility. If the myocardium is already at the apex of the Frank Starling curve, Figure 1. Individual changes in stroke volume (SV) as measured by further stretching would not increase contractility, but with more impedance cardiography with position change in the antepartum period. preload and fixed contractility, SV should increase. The fact that measurements of contractility such as STR, PEP and LVET demonstrated no change with position may also represent too small a sample size or more likely demonstrates the heart’s fixed pregnancy. Whereas the initial research on ICG use in pregnancy contractility at the peak of the Frank Starling curve as preload and was inconsistent and relied on older equations,26–30 recent therefore SV increases. It was somewhat unexpected that CO as updates in the ICG signal analysis software have been made to measured by ICG did not change with maternal position. This may improve accuracy with changes in breathing and allow for be due to the lack of precision as a derived measurement and measurements over fewer cardiac cycles. To date, little data assumptions made it the calculation of CO. Other possible reasons exist on ICG use in pregnancy since the recently updated ICG for the lack of change typically seen by position change may, in software was updated in 1998.19 What does exist is either part, be attributed to the fluid shifts, including positioning of retrospective, has only a single time point or lacks comparison breast tissue with position change. with other cardiovascular assessments such as thermography or We also demonstrated that ICG was able to detect changes echo. Moreover, there are little comparative data on maternal reflecting physiological adaptations occurring over three stages of hemodynamic parameters during labor using ICG and echo.24,30–45 pregnancy from the late AP to the immediate PP period. For Our study is both prospective and longitudinal, and it provides a example, CO measurements significantly decreased over the late comparison with echo evaluations. Furthermore, few ICG studies stages of pregnancy and TFC significantly increased, whereas even report on cardiac function in more than one position and trends in PEP appeared to nadir during labor and increased within only one involves pregnancy.44,46,47 48 h PP while trends in LVET appeared to do the opposite. LVET is Comparisons between our ICG and echo data as they pertain to thought to represents mechanical systole while PEP represents contractility (STR, LVET, PEP, VI and ACI for ICG, and EF and electrical systole. TFC is the inverse of base impedance, which FS for echo) before, during and after labor yielded a number measures all the fluid and soft tissue in the thorax. The observed of statistically significant correlations as well as acceptable increase in TFC likely reflects an increase in intravascular volume, agreement between these two devices. The lack of consistent which would be anticipated in late pregnancy and during labor. agreement at all time points may, in part, be attributed to This includes the pulmonary venous circulation or left ventricular echo’s lack of sensitivity in detecting small changes in EF and FS, preload. If left ventricular preload were increased with a normal especially in healthy participants. Comparisons between left ventricle, you would expect an increase in CO and a decrease

& 2013 Nature America, Inc. Journal of Perinatology (2013), 675 – 680 Impedance cardiography versus echocardiography J Burlingame et al 678 Table 3. Comparison of echo and ICG contractility measurements of the effect of pregnancy stage in the left lateral recumbent supine position with Bland–Altman percentages of points within the conﬁdence intervals

Parameter Antepartum, N ¼ 26 Intrapartum, N ¼ 18 Postpartum, N ¼ 20

STR LVET PEP VI ACI STR LVET PEP VI ACI STR LVET PEP VI ACI

EF 100 91 86 95 91 100 93 93 100 100 94 100 94 94 94 FS 91 95 91 95 95 100 93 93 100 93 94 100 94 94 100 Abbreviations: ACI, acceleration index; echo, echocardiography; EF, ejection fraction; FS, fractional shortening; ICG, impedance cardiography; LVET, left ventricular ejection time; PEP, pre-ejection period; STR, systolic time ratio; VI, velocity index.

Table 4. Comparison of echo and ICG flow and resistance measurements at different pregnancy stages in the left lateral recumbent supine position with Bland–Altman mean differences, confidence intervals and percentages of points within the confidence intervals

Parameter Antepartum Intrapartum Postpartum

SV (ml) 15.1 ( À 29.1, 59.3), 100% 1.5 ( À 28.7, 31.8), 100% À 4.0 ( À 51.6, 43.6), 94% CO (l min À 1) 1.0 ( À 2.9, 4.9), 95% 0.2 ( À 2.2, 2.5), 100% À 0.3 ( À 3.3, 2.8), 88% SVR (dynes s cm À 5) À 141 ( À 782, 500), 100% À 2(À 504, 500), 100% 143 ( À 483, 770), 100% Abbreviations: CO, cardiac output; echo, echocardiography; ICG, impedance cardiography; SV, stroke volume; SVR, systemic vascular resistance.

Table 5. P-values from repeated measures ANOVA and pairwise comparisons of different pregnancy stages

Variable (n ¼ 13) Repeated measures Pairwise comparisons

ANOVA Intrapartum vs antepartum Postpartum vs antepartum Postpartum vs intrapartum

Stroke volume 0.08 0.58 0.03** 0.11 Cardiac output 0.01* 0.83 0.007* 0.055 Vascular resistance 0.15 0.81 0.06 0.26 Acceleration index 0.54 0.33 0.59 0.73 Velocity index 0.46 0.92 0.23 0.32 Systolic time ratio 0.07 0.56 0.03* 0.08 Pre-ejection period 0.15 0.95 0.06 0.11 Left ventricular ejection time 0.12 0.69 0.053 0.22 Thoracic ﬂuid content o0.001* o0.001* o0.001* 0.04** Abbreviation: ANOVA, analysis of variance. *Po0.025 using Bonferoni’s adjustment for multiple comparisons; **Po0.05.

Figure 2. Cardiac output (l min À 1) and thoracic ﬂuid content (k ohm À 1) at different stages of pregnancy with means and s.d.s indicated with bars.

in PEP because of the Frank-Starling effect. The increased PEP and A major limitation of this study was the small numbers of the decreased LVET are consistent with a decline in left ventricular participants. Using the Bland–Altman analysis with a sample size contractility during the IP and immediate PP periods. If there is, in of 13, you can only detect differences in the SV measured by fact, a temporary or subclinical decrease in left ventricular echo versus ICG with 95% limits of agreement of 0.96 times the contractility, this may be a reason why cardiomyopathy and s.d. of the differences between measurements by the two clinical heart failure present most commonly in the immediate PP methods. With larger numbers, subtle differences between echo period. and ICG may have been detected. Another limitation is that

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