Table 2.

Summary of the method used for fetal electroencephalogram (or electrocorticogram) recording and the condition of recording for the 40 eligible studies.

Authors/year (ref)	Electrode type and placement	Mode/frequency	Condition of recording
Studies in human
Thaler et al., 2000 (17)	Two custom-made circular scalp EEG electrodes (suction silicone rubber cups applied by continuous negative pressure) with a central metal probe applied at the occipitoparietal or parietal region (with at least 4 cm between electrodes). FHR recorded with a scalp electrode.	Signals sampled at 250 Hz, stored and displayed by a Cerebro-trac 2500 (SRD Medical Ltd. Shorashim, Israel) using real-time Fourier transform (FFT) algorithm to calculate the power spectrum of fEEG. Epochs length acquisition: 4 s. Band-pass filter: 1.5–30 Hz. Amplifier sensitivity: 200 μV.	Low risk pregnancies in the active stage of labor.
(20, 58)	N/A	FHR, uterine contractions, fetal blood analysis and fEEG recorded polygraphically. Spectral power analysis was performed in real time sequentially and plotted in 30 s intervals continually over the course of the entire observation in waterfall style.	Normal deliveries (n = 20)
Weller et al., 1981 (19)	Flexible electrode minimizing ECG artifact with an incorporated guard ring surrounding the recording sites and forming the indifferent and common electrodes (acting as a short circuit to the fECG). The two electrodes are 23 mm apart and inserted through a 3 cm dilated cervix (after membrane rupture).	Amplifier circuit: microminiature resistors and standard low noise operational amplifier (SF C 2776UC). Input resistance: 2.5 + 2.5 Ohms. Gain: 32 dB. Power requirement ± 5 volts (100 μA). Noise level set at <2 μV peak to peak (1 to 40 Hz).Infrared telemetry used to convey the fEEG to display and record equipment.	Monitoring during the second phase of uncomplicated labor in primigravid mothers with term fetus under epidural anesthetic. Recording in a standard delivery room.
Wilson et al., 1979 (21)	8 channel portable Elena Schonander Recorder.	Continuous recording. Fetal EEG analyzed in 10 s epochs.	High-risk African primigravida mother.
Chik et al., 1979 (22)	N/A	N/A	N/A
Borgstedt et al., 1978 (23)	Same as Rosen et al., 1973b (42)	Same as Rosen and Scibetta, 1970	Selected high risk cases (based on prenatal maternal complication or suspected intrapartum fetal distress)
Nemeadze, 1978 (24)	Simultaneous fetal EEG and ECG recording from fetal head from the moment of the first stage of labor when cervical dilation was 4-6 cm. No further details provided.	N/A	Study of the impact of premature rupture of the membrane in a group of healthy women (n = 60) and a group of women with mild nephropathy (n = 45). fEEG and fECG are recorded simultaneously during labor and correlated to onset of PROM and the Apgar score.
Chik et al., 1977 (25)	2 scalp cup electrodes held by applied suction on fetal head with a central silver or platinum pin avoiding penetration of the fetal skin.	Same as Rosen and Scibetta, 1970	File selection of high-risk infants monitored for at least 1 h during labor.
Revol et al., 1977 (26)	2 scalp cup electrodes held by continuous suction with a central silver pin, placed on the parietal region of the skull.	Continuous recording during labor and after. EEG device: Mingograf EEG 8 Siemens (ink jet print). Filter from frequencies >30 Hz. Band-pass with 0.15 s time constant. Calibration 1 s, 50 μV.	125 cases: normal labor (35), abnormal labor (18), fetal distress (19), under anesthesia (alfatesine n = 21) or ketamine (n = 26).
Sokol et al., 1977 (27)	Same as Rosen et al., 1973b PMID: 4681833	Same as Rosen and Scibetta, 1970	EEG recorded in suspected increased risk deliveries. EEG findings assessed in relation to follow up at 1 year.
Chik et al., 1976a (28)	Same as Rosen et al., 1973b	Same as Rosen and Scibetta, 1970	Same as Rosen et al., 1973b
Chik et al., 1976b (29)	Same as Rosen et al., 1973b	Same as Rosen and Scibetta, 1970	Same as Rosen et al., 1973b
Hopp et al., 1976 (30)	Same as Hopp et al., 1972 (44)	Same as Hopp et al., 1972 (35)	Simultaneous recording of fEEG and CTG in 220 fetuses, (85 cases ultimately included). with some under conditions of intermittent hypoxia due to uterine contractions and after maternal administration of drugs.
Borgstedt et al., 1975 (31)	2 scalp cup electrodes held by applied suction on the fetal head with a central silver or platinum pin avoiding penetration of the fetal skin. Electrodes implanted once cervix dilation reached 2 cm.	Same as Rosen and Scibetta, 1970	Patients selected because of increased prenatal risk or suspected fetal distress during labor.
Chik et al., 1975 (32)	Same as Rosen et al., 1973b	Same as Rosen and Scibetta, 1970	Retrospective evaluation of fEEG recording.
Challamel et al., 1974 (33)	3 Modified Dassault electrode (cup with central pin) placed on the scalp with one placed in parietal position and a minimal distance between electrodes of 4 cm.	EEG device: Mingograf EEG 8 Siemens (ink jet print). Filter from frequencies >30 Hz. Band-pass with 0.15 s time constant. Calibration 1 s, 50 μV. Continuous recording (30 min to 5 h intrapartum). Best derivation exploited.	Monitoring during different conditions of labor (including fetal distress).
Fargier et al., 1974 (34)	Same as Challamel et al., 1974	Same as Challamel et al., 1974. No filter <70 Hz.	Monitoring during different conditions of labor and different drug administrations.
Heinrich and Seidenschnur, 1974 (35)	Same as Rosen et al., 1973 (42)	Intrapartum multimodal fetal monitoring device: RFT Fetal Monitor BMT-504.	One example of EEG recorded in a neonate to show how the new monitor can be used.
Beier et al., 1973 (36)	1 cup electrode consisting of a central needle pin surrounded by a 4 cm disc and two suction grooves connected with a suction device to ensure firm electrode placement over the fetal skull.	1-channel EEG; simultaneous recording of fetal ECG, FHR and intraamniotic pressure channels. Calibration 1 s, 50 μV.	About 30 min duration intrapartum monitoring in 34 fetuses from healthy pregnancies, labor and postnatal outcomes. In 15 fetuses/neonates, the corresponding postnatal recordings were also made.
Carretti et al., 1973 (37)	Plexiglas suction cup with 6 electrodes around its periphery placed on the fetus occiput following >4 cm cervix dilation.	Galileo apparatus allowing multipolar EEG recording.	Comparison of fEEG in healthy mother before and after oxygen administration.
Peltzman et al., 1973 (39)	2 flexible stainless-steel screw electrodes (impedance <400 Ohms in all cases)	FEEG is continuously monitored on a polygraph (Grass instrument Co., Quincy, Massachusetts). Band-pass filter: 1.0 to 35.0 Hz. A PDP-7 computer allows real time analysis and storage of the fEEG before the information is transmitted to a 64-channel analog/digital converter. The fEEG for each 5 s epochs is set to zero mean. Mean fEEG and time integrated fEEG amplitude are also computed. The program then computes a zero line-cross count on the zero-mean fEEG by checking along the wave within each 5 s epoch and recording the line cross each time the polarity changes. Data based upon 12 to 19 continuous 5 s epochs are presented as graphs with plotted points from the beginning of the recording and represent artifact-free analog fEEG.	Uneventful labor and delivery (3 out of 5 were induced labor). Effect of analgesia with meperidine (n = 3) and diazepam (n = 2) or paracervical block (n = 2) evaluated.
Peltzman et al., 1973 (40)	2 flexible stainless-steel bipolar screw electrodes placed 3–4 cm apart of the parietal area of the fetal scalp.	Similar to Peltzman et al., 1973	Uneventful labor with paracervical block (1% mepivacaine) administered
Rosen et al., 1973a (15)	Same as electrodes as Rosen et al., 1970 Electrodes placed along the sagittal suture and between the fontanelles to avoid the forceps blade in forceps birth (over the parietal region for spontaneous birth)	Similar to Rosen and Scibetta, 1970	FEEG during expulsion efforts and during low forceps deliveries are compared to EEG during spontaneous deliveries. Pre-forceps EEG also recorded for comparison.
Rosen et al., 1973b (42)	2 electrodes applied over the parietal and consisting of a silver pin in the center of a lucite disc maintained in place by continuous suction after application with an interelectrode distance of at least 4 cm.	Similar to Rosen and Scibetta, 1970	EEG recording during different labor situations (eventful vs. complicated labor in neurologically abnormal infants).
Hopp et al., 1973 (38)	Same as Hopp et al., 1972 (44)	Same as Hopp et al., 1972 (44)	Simultaneous recording of fetal EEG, fECG and CTG in 37 fetuses during labor in the late first stage and in the stage of active pushing (second stage).
Chachava et al., 1972 (43)	Two fEEG and fECG electrodes placed onto the fetal head, as remotely from each other as possible, fixated using vacuum suction.	N/A	fEEG, fECG and maternal EEG recorded following cervical dilation and rupture of membranes during the first stage of labor.
Hopp et al., 1972 (44)	3 cup electrodes made of a 40 mm silver disc with a 5 mm center pin are used: two biparietal and one on midline, placed and held by suction.	Fetal ECG, CTG and intra-amniotic pressure acquired with an 8-channels EEG device. Artifact free fEEG was achieved when bimodal rejection mode was chosen (i.e., biparietal EEG electrode against a ground).	Simultaneous recording of fEEG and CTG during different labor conditions including normal labor and cardiac decelerations.
Mann et al., 1972 (45)	Two silver disc electrodes consisting of a vacuum contact cup, tube and wire connection and a vacuum electric plug to the vacuum module are placed with membranes ruptured after cervix dilation reaches 3–4 cm. The electrodes are placed up against the vertex about 1 to 2 cm apart.	Serial bipolar EEG are obtained by direct write out on the dual-channel San'Ei electroencephalograph (San'Ei Instrument Co., Div. of Medical System Corp, Great Neck, New York)	Description of the electrode used to record fetal EEG during labor (50 recordings). Specific conditions of recording not documented.
Rosen and Scibetta, 1970 (47)	Two electrodes consisting of a platinum needle embedded in the center of a lucite disc with the firm margin of the disc preventing deep penetration of the needle. Continuous suction is applied within the disc to draw the scalp up to the needle recording point (with possible skin penetration of 1–2 mm). Circular grooves into the lucite disc prevent the skin from occluding the suction. Electrodes implanted as soon as cervical dilation reached 3 cm over the parietal areas.	Bipolar EEG recording using an 8-channel Dynograph Recorder run at 30 mm/s. Time constants are arranged to allow recording wave frequencies between 0.5 and 32 Hz/min. Recording amplitude of 20 μV/cm and 50 μV/cm are used.	125 fetuses recorded during different conditions (normal labor, forceps assisted delivery and following drug administration).
Chachava et al., 1969 (48)	Two fEEG scalp electrodes were held with vacuum suction and placed 2–3 cm apart on the fetal head (after 3–4 cm cervical dilation and ruptured membranes).	Bipolar EEG recorded with either a 4-channel locally made device or an 8-channel EEG device by Orion.	fEEG recorded intrapartum: 20 with normal labor and 10 with complications.
Rosen and Scibetta, 1969 (49)	Two electrodes made of an outer shell in silicone rubber with its periphery circumscribed by a silicon rubber guard ring impregnated with powdered silver (the outer ring is a patient ground) and a platinum needle sheathed in a Teflon tube soldered to a silver plate wire with its distal 2 mm left bare, are used. The electrodes are introduced after membranes ruptured once cervix dilation reached 3 cm. Suction is turned on after the electrode is applied on the fetal head.	Recording in standard EEG fashion with filters admitting wave frequencies between 0.5 and 32 Hz. Paper speed is 30 mm/s recording amplitude at 20 to 50 μV/cm. To document the EEG activity as brain waves, the technique of evoked response to a 34 dB, 35 ms sound (repeated every 4 s) is used.	Fetal EEG during labor (no more detail provided).
Barden et al., 1968 (50)	Skin-clip electrode placed on the presenting vertex.	A summing computer (Mnemotron Corporation CAT-Model 400 B). is used to accentuate fEEG response time locked to an acoustic signal and to cancel non time-locked fECG and random electrical noise signals. FEEG responses were sequentially averaged.	Elective induced labor. FEEG recorded before, during and after the onset of a 1,000 Hz, pure tone of 450 s duration (88 to 105 dB).
Rosen and Satran, 1965 (51)	Metal skin clips soldered to shielded cable, coated with non-conductive plastic glue and filed at their tip to prevent deep scalp penetration and attached to the vertex with a modified uterine packing forceps. Mother grounded to the machine by a strap around the thigh.	Grass Model III portable EEG (Grass Instrument Co., Quincy, Mass).	Normal labor condition studied.
De Haan et al., 1997 (52)	Two pairs of EEG electrodes (AS633-5SSF, Cooner Wire Co., Chatsworth, CA) placed on the parasagittal fetal dura through burr holes (skull coordinates relative to bregma: anterior 5 mm and 15 mm, lateral 10 mm).	The total fEEG intensity is median filtered to remove short-term (<20 min) fluctuations, log transformed to get a better approximation of the normal distribution and normalized with respect to the 12-h baseline. Total EEG intensity, EEG spectral edge (upper 90% of frequency), and cortical impedance are measured in 15-min periods during UCO and in 5-h intervals after the last occlusion. Epileptiform activity and spike detection software (Monitor, Stellate Systems, Quebec, Canada) is used to scan the raw EEG file.	FEEG recorded after UCO with fetuses randomized to one of three groups: group I, repeated total UCO for 1 min every 2.5 min; group II, repeated total UCO for 2 min every 5 min; and group III, no occlusions (sham controls). UCO is repeated until fetal arterial blood pressure had fallen below 2.7 kPa (20 mm Hg) during two successive occlusions, or until fetal blood pressure failed to recover to baseline levels when the next occlusion is due.
Thorngren-Jerneck et al., 2001 (53)	Two EEG electrodes (shielded stainless steel) placed bilaterally over the parietal cortex (10 mm anterior of bregma and 15 mm lateral of midline), inserted through drilled holes in the parietal bone. A subcutaneous reference electrode is placed posteriorly in the midline of the skull.	No detail provided.	16 near-term fetal lambs: 8 lamb fetuses exteriorized and subjected to total UCO in a water bath, four lamb fetuses exteriorized and serving as sham controls and four lamb fetuses immediately delivered after minimal preparation and serving as healthy controls
Kaneko et al., 2003 (54)	Electrodes of Teflon-coated stainless-steel wire (Cooner Wire, Chatsworth, Calif) implanted biparietally on the dura for recording of electrocortical activity.	No details provided.	ECoG recording following repeated UCO for 4 min, every 90 min, and over 6 h (total 4 UCO).
Gerrits et al., 2005 (55)	Two pairs of EEG electrodes (AS633-5SSF; Cooner Wire Co., Chatsworth, CA) placed on the dura over the parasagittal parietal cortex (5 and 15 mm anterior and 10 mm lateral to the bregma), with a reference electrode sewn over the occiput.	Fetal parietal EEG and impedance recorded continuously. Signals are averaged at 1-min intervals and stored to disk by custom software (Labview for Windows; National Instruments Ltd, Austin, TX), running on an IBM compatible computer. The EEG signal is low pass filtered at 30 Hz, and the intensity spectrum and impedance signal are extracted. The raw EEG signal is recorded for off-line detection of seizure events.	Fetal lamb subjected to selective cooling of the head following cerebral ischemia (with one control group)
Frasch et al., 2011 (56)	Stainless steel ECoG electrodes are implanted biparietally on the dura through small burr holes in the skull bone placed ~1–1.5 cm lateral to the junction of the sagittal and lambdoid sutures. The bared portion of the wire to each electrode is rolled into a small ball and inserted into each burr hole to rest on the dura with a small plastic disk covering each burr hole held with tissue adhesive against the skull bone. A reference electrode is placed in the loose connective tissue in the midline overlying the occipital bone at the back of the skull.	ECG and ECoG are recorded and digitized at 1,000 Hz. For ECG, a 60 Hz notch filter is applied. For ECoG, a band pass 0.3–30 Hz filter is used. The ECOG signal is sampled down to 100 Hz prior to analysis. Voltage amplitude and 95% spectral edge frequency (SEF), are calculated over 4 s intervals (Spektralparameter, GJB Datentechnik GmbH, Langewiesen, Germany).	Fetal lamb studied after series of mild, moderate and severe UCO until fetal arterial pH fell below 7.00
Wang et al., 2014 (57)	Fetal instrumentation after exteriorization: a modified FHR electrode with a double spiral placed on the fetal head is used.	A PowerLab system is used for data acquisition and analysis (Chart 5 For Windows, AD Instruments Pty Ltd, Castle Hill, Australia). For fEEG recording, a band pass 0.3–30 Hz filter were used. Prior to analysis, fECoG and fEEG were sampled down to 100 Hz.	FEEG (and fECoG) recorded in near term fetal lamb during repeated UCO.

fECG, fetal electrocardiogram; fECoG, fetal electrocorticogramm; fEEG, fetal electroencephalogram; UCO, umbilical cord occlusion.