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Magnetomyographic Recordings of Pelvic Floor Activity During

Pregnancy and Postpartum: A Novel Non-invasive Approach


Diana Escalona-Vargas Member, IEEE, Sallie Oliphant, Hari Eswaran, Member, IEEE

Abstract— The levator ani muscles (LAM) are integral to imaging, ultrasound) and functional assessment (electromyo-
pelvic floor support and injury to this muscle complex has graphy, clinical strength measures). Both surface and needle
been associated with pelvic floor disorders, but our ability electromyography (EMG) has been used to assess the neuro-
to evaluate their neuromuscular integrity is limited. During
pregnancy, gravidas undergo systemic functional and anatomic muscular function of LAM and has shown good validity and
modifications, including pelvic floor muscular adaptations. interobserver reproducibility [4], [5]. Intravaginal and intra-
Magnetomyography (MMG) is a novel and non-invasive tool to rectal probes have been developed with surface electrodes
passively measure the magnetic fields generated by depolariza- designed to more directly target LAM activity, yet their use
tion activity of muscles and offers a unique method to evaluate requires special care.
the LAM. We collected serial MMG data in a pregnant woman
with singleton gestation. Pregnant woman performed LAM con- Magnetomyography (MMG) is a novel and non-invasive
tractions (Kegels) with intervening rest periods. Kegel signals tool to passively measure the electromagnetic field activity
were isolated by using the frequency dependent subtraction generated by depolarization activity of muscles [6]. MMG
(SUBTR) and independent component analysis (ICA) methods. activities are detectable outside the boundary of the skin
Concurrent body-surface electromyography (EMG) was used to
without any physical contact, thus magnetic fields are not
evaluate for accessory-muscle recruitment by placing bipolar
electrodes on the perineum, abdomen, and thigh. Amplitude disrupted as is usually experience in typical EMG sig-
and spectral-related indicators were computed across moderate nal acquisition. With surface EMG (sEMG), the measured
intensity MMG Kegel epochs: root-mean square (RMS) ampli- electrical activities reaching the skin surface are strongly
tude, power spectrum density (PSD) and relative PSD (rPSD) dependent upon tissue conductivity. It is well known that
in three frequency bands. Indicators were extracted from two
sEMG signals suffer some degree of attenuation by the time
pregnancy recordings and one postpartum. Parameters were
represented in terms of gestation and postpartum weeks. We they reach the surface. MMG allows the interpretation of
observed that postpartum RMS Kegel amplitudes had lower skeletal muscle contraction mechanisms from the magnetic
values than seen in pregnancy. Changes in spectral indicators fields produced by the same ionic currents that give rise
were observed between pregnancy and postpartum. to EMG signals. Thus, MMG is potentially superior in
providing additional details concerning muscle contraction
I. I NTRODUCTION mechanisms and offers a unique method to evaluate the LAM
The levator ani muscles (LAM) are integral to pelvic floor activities. There is limited data on LAM during pregnancy,
support and injury to this muscle complex has been associ- thus the use of this novel MMG technology will improve
ated with pelvic floor disorders, but our ability to evaluate our knowledge of maternal pelvic muscular adaptations and
their neuromuscular integrity is limited. During pregnancy, injury recovery patterns.
gravidas undergo systemic functional and anatomic modi- In this work we provide details about the MMG mea-
fications, including pelvic floor muscular adaptations. The surements and signal processing of data collected during
levator hiatus must relax to allow passage of urine and stool, pregnancy and postpartum. We present indicators extracted
but in women these muscles remarkably are able to stretch from the MMG signals to characterize the LAM activities
and accommodate the passage of the fetal head. Injury to across pregnancy and postpartum period for a single subject.
the LAM complex of the maternal pelvic floor has been
associated with pelvic organ prolapse, prolapse recurrence, II. M ETHODS
and fecal incontinence [1], [2]. Postpartum imaging studies A. Measurements
demonstrate LAM edema in early postpartum which appears
to resolve in many women by later postpartum follow-up [3]. We performed a serial MMG recording of a pregnant
The ramifications of this micro-injury on future pelvic floor woman with singleton gestation at 1st, 3rd trimester and
function and to what degree it is recoverable remains unclear. postpartum. The subject has no identified neurologic condi-
Pelvic floor function in pregnancy has been evaluated tion, connective tissue disorder, or vaginal prolapse at time
by digital palpation, anatomic imaging (magnetic resonance of study enrollment. Recordings were collected under the
protocols approved by the Institutional Review Board and
This work was supported by the U.S. National Institute of Health (NIH) participant provided informed and written consent. MMG
under Grant R21HD091717. data was acquired using the 151-sensor SARA (Supercon-
D. Escalona-Vargas, S. Oliphant and H. Eswaran are with Department ducting Quantum Interference (SQUID) Array for Repro-
of Obstetrics and Gynecology, University of Arkansas for Medical Sci-
ences, Little Rock, AR 72205 USA e-mail: descalonavargas@uams.edu; ductive Assessment) system during voluntary contractions
SSOliphant@uams.edu; eswaranhari@uams.edu. of the LAM (Kegels) with rest intervals. Data was collected

978-1-5386-1311-5/19/$31.00 ©2019 IEEE 1855


with a sampling rate of 1.2kHz. Pregnant woman was in- B. Signal processing for isolating LAM activities
structed to perform LAM contractions (Kegels) generating In our previous work reported in [7] we observed that
subjective small (SmK), moderate (MK), and strong (StK) MMG data was contaminated in majority by synergistic
Kegels each 10s with intervening 10s rest. Additionally, we activation from thigh and abdominal muscles. Contribu-
collected 10s of purposeful isolated abdominal (A) and thigh tions from accessory muscle groups are typical in Kegel
(T) activation. Pregnant woman had a clinical pelvic exam studies [8]. New subject position on SARA device avoids
and transperineal ultrasound for confirmation of ability to the capture of abdominal activities but thigh activities are
perform Kegel contractions. In order to validate that the still detected. We used a frequency dependent subtraction
detected MMG signals corresponded to LAM activation, we (SUBTR) method [9] for attenuation of thigh activities.
utilized simultaneous sEMG to evaluate for accessory muscle We perform the following signal processing steps to
recruitment. EMG electrodes were located on abdomen, isolated the Kegel activities: Data was band-pass filtered
thigh, and perineum in bipolar configuration (see Fig. 1b). between 20-200 Hz using a 4th order Butterworth filter and
Additionally, one ECG sensor was positioned on the chest to notch filtered for ambient noise removal (60Hz). SUBTR
collect the cardiac activity. During the SARA recordings, a algorithm was applied to the MMG data using the matrix
STIM channel was recorded to label the Kegel exercises as: formulation described in [10]. We assumed that thigh activ-
SmK, MK, StK, A, T. This measurement protocol is similar ities are captured on the sensors at the edge of SARA tail.
to our previous work reported in [7] where we characterized To perform SUBTR, we selected as reference signals sensors
the LAM in healthy nulligravid women. But we have made close to the thigh muscles. Fig. 1b shows with brown circles
modifications to our subject positioning protocol to maximize the sensors used as reference data for SUBTR. We computed
the subject proximity to the MMG sensors and to improve independent component analysis (ICA) to clean baseline
our data capture. Fig. 1 shows the new subject position on activities and increase the signal-to-noise ratio (SNR) of
SARA device and position of the sEMG sensors. We selected the MMG data. MMG epochs were extracted with baseline
channel data from lower region of SARA sensor array given correction within window of -3s to +10s with respect to
proximity LAM. the time voluntary contraction start. For the case of sEMG
time series, we performed same pre-processing steps (band-
pass and notch filters) as MMG, and SUBTR was used to
(A)
attenuate the cardiac activity using as reference the data from
the ECG sensor.
C. LAM indicators
Once that MMG epochs were extracted, amplitude and
spectral-related indicators were calculated across moderate
Kegels as follows:
• Root-mean square (RMS) amplitude: a sliding window
approach was used with 200 ms length and overlap of
199 ms [11]. RMS was smoothed using a 100-point
moving average.
• Power spectrum density (PSD): Welch’s method was
(B) used with a sliding window of 1s with 50% overlap.
ECG • Relative power spectrum density (rPSD): PSD values
were divided into three frequency bands [12] defined
as: rPSDL low (20-80Hz), rPSDM middle (80-140Hz),
rPSDH high (140-200Hz). rPSDs were normalized by
A-sEMG the total power.
Descriptive statistics (average and standard deviations)
for each moderate Kegel across SARA sensors from the
MMG
amplitude and spectral metrics were calculated. Indicators
were represented in terms of gestation and postpartum weeks.
P-sEMG
T-sEMG
III. RESULTS AND DISCUSSION
We were able to capture LAM activity from all three
recordings for same subject. We obtained two pregnancy
Fig. 1. (A) Pregnant woman positioned on SARA system. (B) SARA sensor recordings at gestational ages of 14 weeks and 6 days
array (black dots), A (green dots) P (red dots) and T (blue dots) sEMG. ECG
sensors (purple dots). Lower MMG sensors are remarked. Brown circles are
(denoted as 14w6d) and 33w4d, and one postpartum at 6
the sensors used as references for SUBTR method. weeks after delivery (denoted as 6wpp). Subject is 23 years
old, BMI of 27.8 kg/m2 at the time of study entry. Subject
had vaginal delivery at 38w1d.

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MK MK MK SmK MK StK A T 50 14
MMG
MK#1
MCC0 12

400 fT
45 MK#2

Power (T /Hz)*10 30)


MRB1 MK#3

RMS Amplitude


MK#4
MCB0 10
40
MLB1

2
8
MRA1

MLA1 35
6
pregnancy postpartum
20 40 60 80 100 120 140 160sEMG
Time (s) 30 4
14w 33w 6wpp 14w 33w 6wpp

30 mV
A

P 60 60 40
T

55 55 35
20 40 60 80 Time (s) 100 120 140 160
R21pmmg5_14w4d04
50 50 30

rPSD middle (%)

rPSD high (%)


rPSD low (%)
(a) 14w4d
MK MK MK SmK MK StK A T 45 45 25
MMG
40 40 20
MCC0

400 fT
MRB1
35 35 15
MCB0
30 30 10
MLB1 14w 33w 6wpp 14w 33w 6wpp 14w 33w 6wpp
MRA1

MLA1 Fig. 3. Pregnancy and postpartum MMG indicators.

Time (s) sEMG


30 mV

A
Fig. 2 shows the MMG and concurrent sEMG time series
P

T
for the pregnant woman during periods of rest and voluntary
muscle contractions. Dots on the top of the panels denoted
20 40 60 80
Time (s)
100 120 140 160 180 the start of an exercise. As expected, MMG signals corre-
R21pmmg5_33w4d01
sponded with the P (red) sEMG sensor during the Kegel
(b) 33w4d exercises. For all recordings, Kegel activities were 72%, 35%
MK MK MK SmK MK StK A T

MMG
and 22% grater than rest period for StK, MK and SmK,
respectively.
MCC0 MMG
400 fT

Fig. 3 shows the averaged RMS, power, and rPSD values


MRB1
obtained for each MK epoch per gestation and postpartum
MCB0
weeks. Table I shows the average and standard deviations
MLB1
across the four MK epochs of the amplitude and spectral-
MRA1
related indicators. We observed that postpartum RMS am-
MLA1 plitudes had lower (40.56±0.72) LAM MMG activity than
pregnancy (45.91 ±1.71, 43.00±1.71) values. This seems to
20 40 60 80
Time (s)
100 120 140 160
sEMG match of what is observed in previous EMG studies [13]
A where postpartum (vaginal delivery) group had lower EMG
30 mV

P
activity than primigravid and nulliparous groups. Power
T
values are lower for postpartum compared to pregnancy.
20 40 60 80 100 120 140 160
Most of the frequency content of the LAM activities are
Time (s) R21pmmg5_6wkpp
in low (20-80Hz) and middle (80-140Hz) bands. In skeletal
(b) 6w postpartum EMG muscles studies, dominant changes in EMG signal
during sustained contractions are a compression of the signal
Fig. 2. Pregnancy (GA= 14w4d, 33w4d) and postpartum (6w) MMG
recordings (top panels) with simultaneous sEMG (bottom panels) obtained
spectrum toward lower frequencies [14]. We observed only
at rest, voluntary Kegels with modulated intensity (Sm=small, M=moderate, small changes in the rPSDL and rPSDM across gestation and
St=strong), and purposeful isolated abdominal (A) and thigh (T) contrac- postpartum (around 1%), but first MK (red lines in Fig. 3)
tions. Dots on the top of figures indicated when an exercise start (10s
intervals). sEMG electrodes were place on the abdomen (A), perineum (P),
seems to show a major change in the rPSDL and rPSDM
and thigh (T). between gestation and postpartum values. Skeletal muscles
works suggest that frequency shifts have been attributed to
changes in recruitment and synchronization of the motor

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of fiber. H. Eswaran, “Selection of reference channels based on mutual infor-
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biomagnetic signals,” IEEE Transactions on Biomedical Engineering,
TABLE I
2016.
AVERAGE AND STANDARD DEVIATIONS OBTAINED FROM THE [11] C. Auchincloss and L. McLean, “Does the presence of a vaginal
AMPLITUDE AND SPECTRAL - RELATED MK INDICATORS FOR probe alter pelvic floor muscle activation in young, continent women?”
Journal of Electromyography and Kinesiology, vol. 22, no. 6, pp.
PREGNANCY AND POSTPARTUM RECORDINGS . PSD AND RMS UNITS
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ARE (T 2 /H Z )*10−30 ) AND FEMTO T ESLAS , RESPECTIVELY. [12] D. Roman-Liu and M. Konarska, “Characteristics of power spectrum
density function of emg during muscle contraction below 30% mvc,”
Metric 14w 33w 6wpp Journal of Electromyography and Kinesiology, vol. 19, no. 5, pp. 864–
RMS 45.91 (1.71) 43.00 (1.71) 40.56 (0.72) 874, 2009.
Power 10.16 (0.81) 8.71 (0.73) 8.10 (0.32) [13] L. C. Pereira, S. Botelho, J. Marques, D. B. Adami, F. K. Alves,
rPSDL 47.88 (1.43) 49.11 (1.35) 48.59 (0.62) P. Palma, and C. Riccetto, “Electromyographic pelvic floor activity:
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IV. C ONCLUSIONS AND FUTURE DIRECTIONS

This is the first study that uses MMG, a novel and non-
invasive technique, to serially measure LAM activities to as-
sess pelvic floor function during pregnancy and postpartum.
In a single subject, we observed that postpartum RMS MK
amplitudes had lower values than seen in pregnancy. Changes
in spectral indicators were observed between pregnancy and
postpartum. We plan to expand the number of pregnant
women where data will be collected serially. Future work will
add more indicators, such as median frequency, to evaluate
LAM function, injury, and recovery in pregnancy.

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