Electromyographic Response to Exercise in Cardiac Transplant Patients: A New Method for Anaerobic Threshold Determination

DOI 10.1378/chest.111.6.1571 1997;111;1571-1576Chest

 ChicharroSánchez, Violeta Sánchez, Miguel A. Gómez and José L.

Alejandro Lucía, Almudena F. Vaquero, Margarita Pérez, Oscar Determination?Method for Anaerobic Thresholdin Cardiac Transplant Patients : A New Electromyographic Response to Exercise

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Electromyographic Response toExercise in Cardiac Transplant Patients*A New Method for Anaerobic ThresholdDetermination?

Alejandro Lucia, MD, PhD; Almudena F. Vaquero, MD, PhD;Margarita Perez, MD, PhD; Oscar Sanchez, MD, PhD; Violeta Sanchez, MD;Miguel A. Gomez, MD; and Jose L. Chicharro, MD, PhD

The purpose of this study was to investigate the possible use of integrated surface electromyo¬graphy (iEMG) in cardiac transplant patients (CTPs) as a new noninvasive determinant of themetabolic response to exercise by studying the relationship between the iEMG threshold(iEMGT) and other more conventional methods for anaerobic threshold (AT) determination, suchas the lactate threshold (LT) and the ventilatory threshold (VT). Thirteen patients (age: 57±7years, mean±SD; height: 163±7 cm; body mass: 70.5±8.6 kg; posttransplant time: 87±49 weeks)were selected as subjects. Each ofthem performed a ramp protocol on a cycle ergometer (startingat 0 W, the workload was increased in 10 W/min). During the tests, gas exchange data, bloodlactate levels, and iEMG of the vastus lateralis were collected to determine VT, LT, and iEMGT,respectively. The results evidenced no significant difference between mean values of VT, LT, or

iEMGT, when expressed either as oxygen uptake (11.1±2.4, 11.7±2.3, and 11.0±2.8 mL/kg/min,respectively) or as percent maximum oxygen uptake (61.6±7.5, 62.2±7.7, and 59.6±8.2%,respectively). In conclusion, our findings suggest that iEMG might be used as a complementary,noninvasive method for AT determination in CTPs. In addition, since the aerobic impairment ofthese patients is largely due to peripheral limitation, determination of iEMGT could be used toassess the effectiveness ofan exercise rehabilitation program to improve muscle aerobic capacity

in CTPs. (CHEST 1997; 111:1571-76)

Key words: anaerobic threshold; cardiac transplantation; electromyography; exercise

Abbreviations: AT=anaerobic threshold; CTPs= cardiac transplant patients; EMG=electromyography;iEMG=integrated surface electromyography; iEMGT=electromyographic threshold; HR.heart rate; LT^1 lactatethreshold; Vo2=oxygen uptake; Vo2 peak=peak oxygen uptake; VT=ventilatory threshold

T"1 he high survival rates of patients after orthotopic-*- heart transplantation have led many investigatorsto study the cardiorespiratory and metabolic re¬

sponses to exercise of cardiac transplant patients(CTPs).110 In this regard, the anaerobic threshold(AT) has been used as an objective parameter for thedetermination of functional capacity in CTPs.4 It hasbeen reported that in these patients, AT occurs atlower exercise intensities than expected when com-

*From the Unidad de Investigation (Drs. Lucia, Vaquero, Perez,O. Sanchez, and Chicharro), Escuela de Medicina de la Educa¬tion Fisica y el Deporte, Universidad Complutense de Madrid,and the Unidad de Transplante Cardiaco (Drs. V. Sanchez andGomez), Hospital 12 de Octubre, Madrid, Spain.Manuscript received October 2, 1996; revision accepted January21, 1997.Reprint requests: Alejandro Lucia, MD, PhD, Unidad de Inves¬tigacion, Escuela de Medicina de la Educacion Fisica y elDeporte, Facultad de Medicina, PabeUon VI, 5a Planta, Univer¬sidad Complutense de Madrid, 28040 Madrid, Spain

pared either with age-matched control groups ofhealthy individuals2 or with patients who had under¬gone other types of cardiac surgery.11On the other hand, since Wasserman and cowork¬

ers12 originally proposed the AT to predict aerobicendurance capacity, several methods have been re¬

ported for AT determination, based on the determi¬nation of different physiologic parameters such as

expired gas,1314 blood lactate1516 and cat¬echolamines,17 heart rate (HR),18 salivary composi¬tion,19 or the electromyographic (EMG) response ofskeletal muscles to exercise.20-21 Concerning thelatter method, it is known that surface EMG isavailable to quantify the total activity of workingmuscles and that integrated surface EMG (iEMG) isan acceptable method for estimating muscle fatiguenoninvasively. Indeed, an increase in iEMG has beenshown to reflect the recruitment of additional motorunits and an increase in motor unit rate coding as the

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strength of a muscle contraction increases.22 In thisline of thought, several studies have evidenced theexistence of a nonlinear increase in iEMG during theaerobic-anaerobic transition phase in ergometer cy¬cling, indicating that iEMG could be used as a

noninvasive method for AT determination.20'21'23'24Indeed, an iEMG threshold (iEMGT) has beensuggested to occur in the vastus lateralis,20'21'23'25rectus femoris,23 and vastus medialis,23 during incre¬mental tests in a cycle ergometer. Such threshold, inturn, would represent the point where there is an

increased contribution from fast twitch motor unitsto maintain the required energy supply for musclecontraction.2123 Other studies, however, have ob¬served a linear relationship between iEMG andexercise intensity in ergometer cycling.2629To our knowledge, no study has been reported

regarding the iEMG response to exercise in CTPs. Itwas therefore the purpose of our investigation to

analyze the iEMG response of leg muscles (vastuslateralis) of a group of CTPs during an incrementaltest in cycle ergometry. In addition, we aimed to

investigate the possible use of iEMG in these pa¬tients as a noninvasive determinant of the metabolicresponse to exercise by studying the relationshipbetween iEMG response (iEMGT) and that of moreconventional methods for AT determination such as

blood lactate levels (lactate threshold [LT]) andventilatory parameters (ventilatory threshold [VT]).

Materials and Methods

SubjectsThirteen patients (10 male and three female) who had under¬

gone orthotopic cardiac transplantation (age: 57±7 years,mean±SD; height: 163±7 cm; body mass: 70.5±8.6 kg) partici¬pated in this study. W7ritten informed consent was given prior to

participation in the experiments, in accordance with the institu¬tional human subjects guidelines (Escuela de Medicina delDeporte de la Universidad Complutense de Madrid). At the timeof evaluation, the mean posttransplant time of the subjects was

87±49 weeks (range, 13 to 180 weeks). All the patients were

receiving immunosuppressive therapy consisting of cyclosporine,azathioprine, and prednisone, and had no signs of acute rejection.

Study Protocol

Prior to each exercise testing session, patients were familiar¬ized with the equipment and procedures used in this investiga¬tion. All the subjects performed a bicycle ergometer test (Ergo-metrics 900; Ergo-line; Barcelona, Spain) in a thermallymoderate environment (21 to 24°C, 45 to 55% relative humidity).Each of the tests consisted of a ramp protocol, starting at 0 W; theworkload was increased in 10 W/min, and pedaling cadence was

kept constant at 60 to 80 rpm. HRs (beats/min) were continu¬

ously monitored during the tests from modified 12-lead ECGtracings (EK56; Hellige; Freiburg, Germany). Exercise tests wereterminated (1) voluntarily by the subjects, (2) when pedaling

cadence could not be kept at least at 60 rpm, or (3) whenestablished criteria of test termination were met.30

Expired Gas Analysis and Ventilatory Threshold Determination

During the tests, gas exchange data were collected continu¬ously using an automated breath-by-breath system (CPX; Medi¬cal Graphics; St. Paul, Minn), based on a method describedelsewhere.31 The measuring instruments were calibrated beforeeach test and the necessary environmental adjustments were

made. The VT was determined using the criterion of an increasein both the ventilatory equivalent for oxygen and the end-tidalPo2 with no increase of the ventilatory equivalent for carbondioxide.14

Blood Lactate Concentration and LT Determination

Capillary blood samples (50 julL) for the measurement of bloodlactate (YSI 23L; Yellow Springs Instruments; Yellow Springs,Ohio) were taken from fingertips at rest, every 2 min during thetest, and immediately after termination of exercise.The LT was determined by examining the "lactate concentra¬

tion-work load" relationship during the tests, using the methodpreviously described by Weltman and coworkers.32 Thus thegreatest work rate not associated with a rise in lactate concentra¬tion above the baseline was designated as the workload corre¬

sponding to LT.Two independent observers detected LT and VT following the

criteria previously described. If they did not agree, the opinion ofa third investigator was included.

Electrode Placement

The EMGs w?ere recorded from the vastus lateralis using a

bipolar electrode configuration with an interelectrode distance of20 mm. These electrodes were placed over the belly of themuscle approximately at the midpoint between the head of thegreater trochanter and the lateral condyle of the femur.33 Areference electrode was placed equidistant with respect to thedifferential electrodes. Prior to electrode application, the skinwas shaved and abrased using sandpaper to minimize the source

impedance.

EMG Instrumentation and Procedures

Myoelectric signals during exercise tests were amplified withband-pass filtering (250 Hz) and recorded on a digital datarecorder (ME3000P; Mega Electronics Ltd; Kuopio, Finland).Data were digitized at a sampling frequency of 1 kHZ, and theiEMG was calculated at every 2-s interval by the use of a

computer (486DX66; Investronica; Washington). In each subject,we obtained a graphic representation of the EMG recording,representing the increase in muscle electrical activity (iEMG, inmicrovolts) during the ramp test, as exercise intensity graduallyincreased with time. Figure 1 provides an example of the EMGresponse of one subject.

iEMGT Determination

The iEMG data against time during each exercise test were

fitted mathematically to two straight lines by linear regression todetermine the breakpoint (iEMGT) of the linear relationshipbetween iEMG and time of exercise (that is to say, iEMG againstwork rate) (Fig l).34 The exercise time (s) corresponding to the

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120

100

>3 80

CD

IU60

40

20

iEMGT

100 200 300 400

Time (s)Figure 1. Example of EMG response in one subject. Each data point represents a value of iEMG,recorded at every 2-s interval. The iEMG data against time were fitted mathematically to two straightlines by linear regression.

iEMGT was therefore determined as the crossing point of thetwo lines.

Comparison Among VT, LT, and iEMGT

Each individual value of XT1, LT, and iEMGT corresponded toa certain time point (work rate) during the tests, which in turnelicited a certain value of Vo2. Therefore, to compare the exerciseintensity at which all three thresholds occurred, mean values ofVT, LT, and iEMGT were expressed both in oxygen uptake (Vo2)(in mL/kg/min) and in percent peak oxygen uptake (Vo2 peak).

Peak Values

Peak values of Vo2, respiratory exchange ratio,minute ventilation, HR, and lactate averaged 18.3±4.8mL/kg/min, 1.06±0.1, 53.3±25.4 L/min, 125±17beats/min, and 4.7±1.7 mmol/L, respectively. Thesubjects reached an average value of peak work of87.0±44.2 W (range: 46 to 227 W) at the end ofexercise.

Data AnalysisResults were expressed as mean±SD. Repeated measures of

analysis of variance were used to determine if there was a

significant difference (p<0.05) among mean values of VT, LT,and iEMGT when expressed in Vo2 (mL/kg/min) and in percentVo2 peak. In addition, the relationship among VT, LT, andiEMGT was assessed using the Pearson correlation coefficient atthe 0.05 level of significance.

Results

Exercise Termination

All patients voluntarily terminated the exercisetests due to either leg or general fatigue, or dyspnea,and not because of altered hemodynamic responses(ie, ECG abnormalities). The average duration oftests was of 491 ±115 s.

Comparison Among LT, VT, and iEMGT

Using the methods described above, VT and LTcould be detected in 100% (n=13) and 85% (n= 10)of subjects, respectively. Average values of LT oc¬

curred at a blood lactate concentration of 1.5 ±0.5mmol/L. However, an EMG threshold response was

identified in 100% of the subjects.Mean values of VT, LT, and iEMGT expressed

in Vo2 (mL/kg/min) and in percent of Vo2 peakare expressed in Table 1. No significant differ¬ences (p<0.05) were found among mean values ofVT, LT, or iEMGT when expressed either as Vo2 or

as %Vo2 peak.Finally, all three parameters were significantly

correlated (p<0.05) when expressed as Vo2 or as

%Vo2 peak (Table 2).

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Table I.Mean Values ofVT, LT, and iEMGT*

Vo2 mL/kg/min Wo9 Peak

VTLTiEMGT

11.1 ±2.411.7 ±2.311.0 ± 2.8

61.6 ± 7.562.2 ± 7.759.6 ± 8.2

*All the results are expressed as mean±SD. No significant differ¬ences existed between means (p<0.05).

Figure 2 shows an example of determination of VT,LT, and iEMGT, respectively, in the same subject.

Discussion

Peak Values

The low values ofVo2 peak (18.3±4.8 mL/kg/min)obtained in our investigation are in agreement withthose reported for CTPs in previous studies, at abouttwo-thirds of those of age-matched control sub¬jects.11011 Lactate levels at peak exercise, on theother hand, were also similar to those reported byother authors.156 Finally, mean values of peak HRs(125±17 beats/min) were similar to those reportedin other studies.78 Some authors, however, havereported higher values of Vo2 peak and peak HR in

younger CTPs (mean age younger than 50 years).2-39In addition, our protocol did not include a warm-upperiod. During warm-up periods, indeed, circulat¬ing catecholamine levels might increase before thebeginning of testing, leading to higher HRs duringa test.9

Ventilatory and Lactate Thresholds

In our investigation, the %Vo2 peak correspondingto the VT and to the LT (approximately 62%) was

higher than the values reported in previous stud¬ies,15 in the range of 50 to 60% Vo2 peak. Suchdifference, in turn, might be partly explained by theramp protocol used in our study. During such typesof protocols, indeed, the blood lactate response toexercise might be delayed.35 In addition, our subjects(mean, 57 years) were, in general, older than thoseselected in previous research with CTPs. In thisregard, it has been suggested that the pattern ofrecruitment of fast glycolytic fibers might be alteredwith aging, resulting in a delayed lactate responseduring exercise.36 In a study recently reported by us,indeed, the LT of a group of CTPs with similarcharacteristics occurred at 64% Vo2 peak.'However, no significant differences were noted

between VT and LT, in accordance with the originalwork conducted by Wasserman37 and with the find¬ings of previous research with CTPs.1

EMG Response and AT

To our knowledge, this is the first report to analyzethe EMG response of CTPs during incrementalcycle ergometry. Previous studies with healthy indi¬viduals have evidenced the occurrence of a point(the "iEMGT") where the increase of iEMG ofquadriceps muscles becomes nonlinear during suchtype of exercise.20'2334 This iEMGT, in turn, hasbeen shown to occur during the transition fromaerobic to anaerobic metabolism, at similar exerciseintensities to that of the AT.202324 Indeed, theiEMGT might occur as a result of a change in thepattern of motor unit recruitment from predomi¬nantly slow-twitch motor units to fast-twitch motorunits, which could contribute to the accumulation ofcirculating lactate during exercise.20'21-23'24 TheiEMGT has therefore been suggested as an alterna¬tive, noninvasive method for AT determination.2024Our results are in agreement with those of previ¬

ous studies with healthy subjects, since no significantdifferences were evidenced between the exerciseintensity corresponding to the iEMGT and thatcorresponding to the AT (determined both withventilatory parameters and blood lactate concentra¬tion). It follows that iEMG might represent a com¬

plementary, noninvasive method for AT determina¬tion in this population group. Furthermore, thismethod might be used to study the metabolic re¬

sponse of CTPs to exercise. A major limitation of ourfindings, however, comes from the fact that we didnot study the test-retest reliability of AT determina¬tion with iEMG in CTPs. Thus, new research is stillneeded in this regard to further assess the validity ofiEMG for AT determination.

Clinical ImplicationsPeripheral limitation is one of the factors respon¬

sible for the aerobic impairment of CTPs.10 In thisperspective, determination of iEMGT might repre¬sent a valuable tool for assessing the effectiveness ofan exercise rehabilitation program to improve mus¬

cle capacity in CTPs. A shift of iEMGT to a higherpercentage of Vo2 peak, indeed, should be expected

Table 2.Correlation Coefficients Among VT, LT, andiEMGr, Expressed as Vo2 (mL/kg/min) or as %Vo2

Peak*

VT LT

VT

iEMGT 0.89 (Vo2)0.76 (%Vo2peak)

0.96 (Vo2)0.91 (%Vo2peak)0.88 (Vo2)0.74 (%Vo2peak)

*p<0.05 for all correlations.

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iEMG friV)120

1001-80

60

40

20

0

VE*V021VE-VCCV

40

35

30

3 Lactate (mM«l"

25K

20

16

14

12

H 10

8

6

4

2

0

V02 (ml*kg"1 .min"1)

Time (min)

Figure 2. Example of determination of LT, VT, and iEMGT in one subject. The values of Vo2reported during the test are also included.

with a successful exercise program, reflecting an

improvement in muscle utilization of aerobic metab¬olism and an attenuation of peripheral limitations.

In conclusion, our results suggest that iEMGrepresents a valid, noninvasive method for AT deter¬mination in CTPs, and thus a complementary tool forassessing the overall functional capacity of thesepatients. Further research, however, is necessary toevaluate the practical implications of our findings.

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DOI 10.1378/chest.111.6.1571 1997;111; 1571-1576Chest

Sánchez, Violeta Sánchez, Miguel A. Gómez and José L. ChicharroAlejandro Lucía, Almudena F. Vaquero, Margarita Pérez, Oscar

Patients : A New Method for Anaerobic Threshold Determination?Electromyographic Response to Exercise in Cardiac Transplant

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