British Journal of Obstetrics and Gynaecology October 1994, Vol. 101. pp. 866-870

OBSTETRICS

Antenatal fetal magnetocardiography : a new method for fetal surveillance? ANDREW QUlNN Senior Registrar, ANDREW WEIR Consukant (Neurophysiology), U M A SHAHANI Physiologist, * R H O D E R I C K B A I N Physicist, *PETER MAAS Physicist. *GORDON DONALDSON Professor (Physics) Wellcome Biomugtieti.sni Unit. Southern Generul Hospitul; * the Superconducting Device Group, Struthclyde University. Glusgow

ABSTRACT Objective To establish the reliability of fetal magnetocardiography as a method of measuring the

Design A prospective study.

Setting Wellcome Biomagnetism Unit, Southern General Hospital.

Subjects One hundred and six low risk pregnant women at 20 to 42 weeks gestation.

Main outcome measures Success in obtaining QRS complexes, P waves and T waves. Correlation of time intervals with fetal outcome.

Results The technique was acceptable to pregnant women. A QRS complex was successfully demonstrated in 68 (67 "/o) of the unaveraged traces. Using off-line averaging techniques on these 68 cases, P waves were obtained in 75 YO and T waves in 72 YO. Although good quality traces were obtained throughout the range of gestational ages, in general it was more difficult below 28 weeks. QRS duration (R2 = 7 %, P = 002) demonstrated a positive linear correlation with increasing gestation. Of the 35 (51 YO) cases with umbilical vein pH analysis available, only one result was less than 7.2. No significant relation was found between measurements of the fetal waveforms and the pH results.

Conclusion The technique of fetal magnetocardiography provides a significant advance in the technological field for the demonstration of QRS complexes and the full PQRST waveforms in gestations from 20 weeks onwards. With further technical improvements the clinical impact of this technique can be assessed more fully.

time intervals of the fetal heart during the antenatal period.

Fetal cardiac measurements have frequently been used for both antenatal and intrapartum fetal surveillance. Recording of the fetal electrocardiogram (ECG) using maternal electrodes has been unsatisfactory because of the low signal to noise ratio and interference by the large amplitude maternal ECG field. Thus, only the QRS complex has been detected reliably and antenatal analysis has concentrated on the R-R intervals and their variance. In addition the amplitude of the fetal complexes diminishes from 27 to 35 weeks gestation, because of the insulating properties of the vernix caseosa on the fetal skin (Oostendorp et at. 1989). Attempts to detect a full fetal ECG waveform by removal of the maternal signal using spatial filtering did not produce a significant increase in fetal waveform detail (van Oosterom 1986).

Analysis of the fetal ECG during labour by direct recording via scalp electrodes has concentrated on rate

Correspondence: Dr A. Quinn, Southern General Hospital, 1345 Govan Road, Glasgow G51 4TF, UK.

changes and variability. Analysis of specific fetal ECG components has been suggested for fetal surveillance, as animal studies have demonstrated that ST segment elevation and peaked T waves with the resultant increased T to QRS ratio are associated with hypoxia (Rosen & Isaksson 1976). However, observation of the T wave has proven to be difficult and the results of the preliminary clinical studies have been quite variable. ST waveform changes have been reported to have a significant cor- relation with both abnormal fetal heart rate patterns (Pardi et al. 1974; Lilja et al. 1985), and scalp pH (Johanson et al. 1992) and umbilical pH (Jenkins et al. 1986) measurements. However, other studies have not confirmed these relations (Newbold et at. 1991 ; Murphy et al. 1992).

An alternative technique for the detection of electrical events in the fetal heart is fetal magnetocardiography (MCG) where the magnetic field set up by the intracellular current density within the fetal heart is recorded non- invasively using a Superconducting Quantum Interference

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A N T E N A T A L F E T A L M A G N E T O C A R D I O G R A P H Y FOR F E T A L S U R V E I L L A N C E 867

Device (SQUID) coupled to a gradiometer. Fetal MCG has notable theoretical advantages over antenatal fetal ECG recording. Maternal MCG complexes are less evident due to the more rapid fall off of the magnetic field with distance from source than the electrical equivalent. In addition, the electrically insulating effect of the vernis caseosa, which has a resistance about a factor of lo6 higher than that of the surrounding tissue, has no apparent effect on fetal MCG.

The first adult MCG was recorded in 1963 (Baule & McFee 1963) and the first fetal QRS complex recorded in 1974 (Kariniemi et al. 1974). A single averaged PQRST complex was reported by Dunajski and Peters (1992). More recently, again using averaging techniques and studying 11 women at 30 to 40 weeks' gestation, fetal QRS complexes were recorded in nine and full PQRST complexes in four (Weir et al. 1993). We therefore undertook a larger study of fetal MCG recordings in 106 normal pregnancies from 20 to 42 weeks' gestation, to determine the success rate of the technique and form some initial assessment of its potential clinical value.

Subjects and methods One hundred and six consecutive women with a singleton pregnancy attending a low risk antenatal clinic over a six- month period were recruited with informed written consent. The study was approved by the hospital Ethics Committee.

The subject removed any metal objects from her person and was then positioned on an adjustable bed with a 30" left lateral tilt. The room itself was eddy screened (Bain et al. 199 1) which excluded external magnetic interference. The fetal lie and presentation were determined by palpation and, following auscultation of the fetal heart, the tip of a single channel second order neuromagnetometer (BTi Model 60 1, San Diego, California, USA) was placed 2 to 3 cm above the maternal abdomen at the position where the QRS signal was found to be at its maximum. The neuromagnetometer output was amplified further and the analogue bandpass was filtered (0.03- 100 Hz, single pole high and low pass) using a PAR Model 113 preamplifier (,Princeton Applied Research, Princeton, New Jersey, USA).

Recordings were made in two ways. Sequential 9-s epochs were stored on a personal computer via an analogue-to-digital processor board. At the same time several segments of 5-min duration were stored on tape (FM recorder, SE 84, KUDELSKI SA, Switzerland) for subsequent off-line analysis using the motor unit potential averaging algorithm of a clinical electromyography system (Medelec Sapphire Premiere, Woking, Surrey, UK). Averaging was initiated by a manually controlled voltage level trigger on the R wave. The number of averages required to define the full PQRST complex varied from 15 to 50 depending on the signal to noise ratio. All averages were repeated at least once to check reproducibility.

A recording of the maternal MCG with the same apparatus moved over the maternal chest wall was made at the end of each session.

The outcome of the pregnancy as regards the gestation

at delivery, mode of delivery and indication for any intervention in labour was reviewed. The immediate neonatal condition was assessed by Apgar scores and umbilical vein pH analysis.

Results Of the original 106 subjects recruited into the study 64 (63%) were nulliparous and their mean age was 26 (SD 4.5) years (range 17-35). The gestational age at the time of recording ranged from 20 to 42 weeks (mean 32, SD 5). Of the total, four withdrew before any recording was taken; two because of a feeling of claustrophobia underneath the neuromagnetometer and two because of light-headedness when lying on the bed, despite the lateral tilt. Thus in total 102 fetal MCGs were attempted and a QRS complex was successfully demonstrated in the unaveraged recordings of 68 (67%). Table 1 shows that successful recording of the QRS complex increased with gestation from 43 % in the 20 to 24-week group to 83 % in the 37 to 42-week cohort. However, good quality rec- ordings were obtained throughout the range of gestations (Fig. 1). With care in choosing sensor placement, maternal MCG signals were absent from the recordings.

Using off-line averaging techniques (Fig. 2) we detected a P wave in 51 (77 %) and a T wave in 49 (72 %) of the 68 traces. The time intervals of the components of the fetal MCGs were calculated and the results are shown in Table 1 for five subgroups divided according to gestational age at the time of the recording. The PR interval was defined as the duration from the beginning of the P wave to the beginning of the QRS complex and the QT interval as the duration from the beginning of the QRS complex to the end of the T wave.

Amongst the 68 recordings where at least a QRS complex had been obtained, the mean gestation at delivery was 39 (SD 2) weeks (range 34 to 42) and the mean interval from fetal MCG recording until delivery was 47 (SD 34) days (range 1 to 126).

Using simple linear regression analysis, QRS duration (R2 = 7%, P = 0.02, n = 68) was found to increase significantly with increasing gestation. A similar trend was evident for both the PR interval (R2 = 5%, P = 006, n = 51) and the QT interval (R2 = 5 % , P = 0.07, n = 49) but it was not statistically significant.

Six women (9%) had a caesarean section delivery and 21 (31 %) an instrumental delivery. Obstetric intervention was performed in nine cases on account of fetal distress in labour (diagnosed on the basis of an abnormal FHR pattern and a scalp pH measurement less than 7.25). Two babies had Apgar scores of less than 5 at 1 min but in both cases the scores were normal at 5 min. The mean umbilical vein pH was 7.3 (SD 0.1, range 7.18 to 7.4, n = 35). Only one pH was less than 7.2 and this baby had a normal Apgar score at 5 min following resuscitation.

Overall no significant relationship was found between the waveform intervals and umbilical vein pH. A sub- analysis was performed on the 20 cases where the fetal MCG had been recorded within 14 days of delivery but once again the results were not statistically significant : PR interval (Ra = 43%, P = 0.1, n = 6), QT interval

868 A. Q U I N N ET AL.

Table 1. Success rate in obtaining a QRS complex with fetal magnetocardiography and the time intervals of the averaged waveforms. Values are given as mean (SD); the range is given in parentheses below the mean (SD). Also given are the results of ECGs performed at different gestations taken from the literature.

Total Gestation success rate PR interval QRS duration QT interval (weeks) n (%) (ms) (ms) (ms)

Fetal magnetocardiography 20-24 14 (43)

25-28 19 (53)

29-32 26 (73)

33-36 19 (68)

37-42 24 (83)

TOTAL 102

Fetal electrocardiography 16-23* 13

29 - 30** 20

> 32t 21

Term: 126

n = 6 71 (15) (45-86) n = 7 75 (21) (39- 104) n = 13 73 (16)

n = 10 80 (24)

n = 15 89 (26)

n = 5 1 (50 Yo)

(36- 104)

(45-1 14)

(55- 143)

n = 13 90 (6) -

n = 21 107 (33) n = 126 96 (4.3)

n = 6 43 (9) (32-57) n = 10 40 (8) (28-54) n = 19 41 (11) (26-59) n = 13 49 (10) (3 5 - 63) n = 20 47 (9) (31-63) n = 68 (67 Yo)

n = 13 30 (3) n = 20 44 (4.1) n = 21

n = 126 54 (3.2)

46 (3)

n = 5 157 (28)

n = l 175 (38)

n = 11 205 (44)

n = 1 1 198 (48)

n = 15 196 (44)

n = 49

(121 - 195)

(144-255)

( 143 -293)

(116-251)

(1 32-297)

(48 Yo)

n = 13 300 (1 1) -

n = 2 1 255 (28) -

* Gennser et al. (1968); ECGs obtained directly from fetuses during termination of pregnancy by hysterotomy, mean (SEM). ** Brambati & Pardi (1980); external fetal ECG. t Abboud et al. (1990); maternal ECG waveform was subtracted from the fetal ECG in their technique.

Lewinsky et al.-(1992); ECGs taken during labour.

(Rz = 10 %, P = 0 3 , n = 6) and QRS duration (R2 = 30 %, P = 0.1, n = 7). Similarly for birthweight: PR interval (R2 = 6%, P = 0.7, n = 16), QT interval (R2 = 6%, P = 0.4, n = IS) and QRS duration (R2 = 6%, P = 0 2 , n = 20).

Discussion The fetal MCG technique was generally acceptable to the pregnant subjects, being non-invasive and performed in a comfortable clinical environment. Successful recordings of the QRS complex in 67% of cases attempted were an encouraging result. Although good quality fetal MCG traces were obtained from 20 to 40 weeks' gestation, in general it was a more difficult task before 28 weeks. However, recording with a subject at o r close to term was no guarantee of success, possibly due to the increased frequency of significant uterine activity resulting in high noise levels.

Fetal MCG provides for the first time an accurate method of recording PQRST complexes at any gestation

after 20 weeks, including the window at 27 to 35 weeks gestation when the amplitude of a fetal ECG recorded electrically would be significantly diminished. The tracing of a full fetal MCG complex allows the calculation of measures such as the QT interval, thought by some in the intrapartum ECG to relate to hypoxia (Symonds 1971). As there was only one case in the study with an umbilical cord vein pH less than 7.25 it is impossible to comment on any potential relationship between the time constants of the fetal MCG and fetal acidosis. Although it was not confirmed in this study, in the past a relationship between QRS duration and birthweight has been demonstrated and has even been suggested as a method for the antenatal prediction of birthweight (Brambati & Pardi 1980).

The normal values in Table 1 are in reasonable agreement with measurements made in the past using the fetal ECG (Table 1). The value of calculating measure- ments of amplitude from an antenatal fetal ECG is questionable (Pardi et a/. 1984), as the cardiac currents do not leave the fetus through fixed pathways and the

ANTE N A T A L F E T A L M AG NE TO CAR D I O G R A P H Y F O R FETAL s u R v E I L L A N c E 869

--

. 4’ . 5 ’ . .

Field, lT

WDO

Field, fr

Fig. 1. Examples of unaveraged fetal MCG (trace 01) and maternal MCG (trace 02) recordings at (a) 20, (b) 24, (c) 30 and (d) 40 weeks gestation.

c . ‘

I .

Fig. 2. Example of an averaged (the average of 30 readings) PQRST complex (P and T waves inverted) produced from a fetal MCG at 38 weeks’ gestation. A single division is 50 ms on the x axis and 1 picotesla on the J’ axis.

topographical relationship between the fetal heart and the recording electrodes is not known. Although the effects of tissue conductivities are theoretically less with the fetal MCG than with fetal ECG, Oostendorp & van Oosterom (1991) have demonstrated that the fetal MCG waveform is affected both by the changes in the conductive medium and by the actual geometry (fetal position).

In the unaveraged fetal MCG recordings only a few cases were good enough to be used as a rhythm strip. Traces of this quality are of particular interest as they could serve as an adjunct to ultrasonic techniques in the assessment of suspected second and third degree congenital heart blocks. In cases where only the QRS complex can be demonstrated the use of fetal MCG will be limited to measurements based on QRS duration or R-R intervals. The correlation between abnormal variability of the fetal heart period and suboptimal fetal outcome has been established both intrapartum (Street et al. 1991) and

870 A. Q U I N N ET AL.

antenatally (Ribbert et al. 1990), and measurement by fetal MCG from as early as 20 weeks gestation of the true beat-to-beat variability could be an advantage in bio- physical fetal assessment.

Finally the size of the R waves at 1 to 4 picoteslas (pT) are within the sensitivity range that might be attainable with high T,SQUIDS. These devices have the potential advantages of being cheaper, smaller and able to record in an unshielded environment. Assessment of this technology at any hospital clinic is thus a realistic prospect in the near future.

In summary, fetal MCG provides a significant advance in the technology available for recording the antenatal fetal heart giving reliable detection of the QRS complex from 20 weeks onwards and using simple averaging obtaining the full PQRST waveform in a substantial number of subjects. If the acquisition methods can be made more portable and the analysis techniques improved, the clinical impact of this technique may be fully assessed.

Acknowledgment We would like to thank the obstetric consultants of the Southern General Hospital, Glasgow, who allowed us to study their patients. A.Q. was funded by the Institute of Neurological Sciences Research Trust, Glasgow. The Wellcome Trust funds the Wellcome Biomagnetism Unit.

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15-18.

Received 4 February 1994 Accepted 19 April 1994