Monitoring Fetal Electroencephalogram Intrapartum: A Systematic Literature Review

Aude Castel, Yael S Frank, John Feltner, Floyd B Karp, Catherine M Albright, Martin G Frasch, Aude Castel, Yael S Frank, John Feltner, Floyd B Karp, Catherine M Albright, Martin G Frasch

Abstract

Background: Studies about the feasibility of monitoring fetal electroencephalogram (fEEG) during labor began in the early 1940s. By the 1970s, clear diagnostic and prognostic benefits from intrapartum fEEG monitoring were reported, but until today, this monitoring technology has remained a curiosity. Objectives: Our goal was to review the studies reporting the use of fEEG including the insights from interpreting fEEG patterns in response to uterine contractions during labor. We also used the most relevant information gathered from clinical studies to provide recommendations for enrollment in the unique environment of a labor and delivery unit. Data Sources: PubMed. Eligibility Criteria: The search strategy was: ("fetus"[MeSH Terms] OR "fetus"[All Fields] OR "fetal"[All Fields]) AND ("electroencephalography"[MeSH Terms] OR "electroencephalography"[All Fields] OR "eeg"[All Fields]) AND (Clinical Trial[ptyp] AND "humans"[MeSH Terms]). Because the landscape of fEEG research has been international, we included studies in English, French, German, and Russian. Results: From 256 screened studies, 40 studies were ultimately included in the qualitative analysis. We summarize and report features of fEEG which clearly show its potential to act as a direct biomarker of fetal brain health during delivery, ancillary to fetal heart rate monitoring. However, clinical prospective studies are needed to further establish the utility of fEEG monitoring intrapartum. We identified clinical study designs likely to succeed in bringing this intrapartum monitoring modality to the bedside. Limitations: Despite 80 years of studies in clinical cohorts and animal models, the field of research on intrapartum fEEG is still nascent and shows great promise to augment the currently practiced electronic fetal monitoring. Prospero Number: CRD42020147474.

Keywords: EEG; electrocorticogram; fetus; infant; labor; magnetoencephalogram; neonates.

Copyright © 2020 Castel, Frank, Feltner, Karp, Albright and Frasch.

Figures

Figure 1
Figure 1
PRISMA flow diagram summarizing the study selection process and the number of studies ultimately deemed eligible to be included in the meta-analysis.
Figure 2
Figure 2
(A) Simultaneous recording of fECG and fEEG. Artifacts from fECG effect on fEEG can be identified by recording both traces simultaneously. From Hopp et al. (44). (B) Intra and post-partum fetal/neonatal EEG recordings showing the great similarity between both traces. From Hopp et al. (44). EEG, electroencephalogram. (C) Cardiotocogram (top) and fEEG (bottom) recorded during early cardiac deceleration. The fEEG pattern represents the change during contractions with high amplitude low-frequency waves and the recovery once the contractions ceased. From Hopp et al. (44). fEEG, fetal electroencephalogram. (D) Simultaneous recording of fECG (top trace), two-channel fEEG (middle two traces), and FHR (bottom trace). This figure shows fEEG changes during severe variable deceleration. The fEEG trace shows waves of low amplitude and near isoelectricity as well as intermittent spike potentials between contractions. From Hopp et al. (30). fECG, fetal electrocardiogram; fEEG, fetal electroencephalogram; FHR, fetal heart rate.
Figure 3
Figure 3
Emergence of EEG-FHR pattern in a fetal sheep model. A representative 10 min recording made during the early stage of severe umbilical cord occlusions (UCOs) at a pH of about 7.2 and about 60 min prior to pH dropping to

Figure 4

FEEG recording from the standard…

Figure 4

FEEG recording from the standard fetal scalp electrode during the first stage of…

Figure 4
FEEG recording from the standard fetal scalp electrode during the first stage of labor. A period of 10 min is shown with fEEG tracing (bottom) filtered 0.5–12 Hz and the corresponding power spectral analysis (top left) and wavelet transform (top left) to demonstrate the time-frequency behavior of fEEG. Note switching between delta and alpha-band activity. The X-axis shows time, with each segment corresponding to 0.5 min for a total of 10 min. Signal processing was performed in EEGLAB using Matlab 2013b, MathWorks, Mattick, MA. fEEG: fetal electroencephalogram.

Figure 5

Suggested study protocol. Fetal EEG…

Figure 5

Suggested study protocol. Fetal EEG recording during labor will be followed by cord…

Figure 5
Suggested study protocol. Fetal EEG recording during labor will be followed by cord blood measurements at birth to determine the degree of acidemia and the neonatal morbidity score. FSE, fetal scalp electrode; EEG, electroencephalogram; HR, heart rate.
Figure 4
Figure 4
FEEG recording from the standard fetal scalp electrode during the first stage of labor. A period of 10 min is shown with fEEG tracing (bottom) filtered 0.5–12 Hz and the corresponding power spectral analysis (top left) and wavelet transform (top left) to demonstrate the time-frequency behavior of fEEG. Note switching between delta and alpha-band activity. The X-axis shows time, with each segment corresponding to 0.5 min for a total of 10 min. Signal processing was performed in EEGLAB using Matlab 2013b, MathWorks, Mattick, MA. fEEG: fetal electroencephalogram.
Figure 5
Figure 5
Suggested study protocol. Fetal EEG recording during labor will be followed by cord blood measurements at birth to determine the degree of acidemia and the neonatal morbidity score. FSE, fetal scalp electrode; EEG, electroencephalogram; HR, heart rate.

References

    1. Rees S, Inder T. Fetal and neonatal origins of altered brain development. Early Hum Dev. (2005) 81:753–61. 10.1016/j.earlhumdev.2005.07.004
    1. Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. (2008) 371:261–9. 10.1016/S0140-6736(08)60136-1
    1. James SL, Abate D, Abate KH, Abay SM, Abbafati C, Abbasi N, et al. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: a systematic analysis for the global burden of disease study 2017. The Lancet. (2018) 392:1789–858. 10.1016/s0140-6736(18)32279-7
    1. Liu L, Oza S, Hogan D, Perin J, Rudan I, Lawn JE, et al. . Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet. (2015) 385:430–40. 10.1016/S0140-6736(14)61698-6
    1. Parer JT, King T. Fetal heart rate monitoring: is it salvageable? Am J Obstet Gynecol. (2000) 182:982–7. 10.1016/S0002-9378(00)70358-9
    1. Low JA. Determining the contribution of asphyxia to brain damage in the neonate. J Obstet Gynaecol Res. (2004) 30:276–86. 10.1111/j.1447-0756.2004.00194.x
    1. Low JA, Killen H, Derrick EJ. Antepartum fetal asphyxia in the preterm pregnancy. Am J Obstet Gynecol. (2003) 188:461–5. 10.1067/mob.2003.37
    1. Shepherd E, Middleton P, Makrides M, McIntyre SJ, Badawi N, Crowther CA. Antenatal and intrapartum interventions for preventing cerebral palsy: an overview of Cochrane systematic reviews. Cochrane Database Syst Rev. (2016). 10.1002/14651858.CD012077
    1. Clark SL, Hamilton EF, Garite TJ, Timmins A, Warrick PA, Smith S. The limits of electronic fetal heart rate monitoring in the prevention of neonatal metabolic acidemia. Am J Obstet Gynecol. (2017) 216:163.e1–163.e6. 10.1016/j.ajog.2016.10.009
    1. Cahill AG, Mathur AM, Smyser CD, Mckinstry RC, Roehl KA, López JD, et al. . Neurologic injury in acidemic term infants. Am J Perinatol. (2017) 34:668–75. 10.1055/s-0036-1597135
    1. Frasch MG. Saving the brain one heartbeat at a time. J Physiol. (2018) 596:5503–04. 10.1113/JP275776
    1. Gibbons L, Belizán JM, Lauer JA, Betrán AP. The global numbers and costs of additionally needed and unnecessary caesarean sections performed per year: overuse as a barrier to universal coverage. World Health. (2010). Available online at:
    1. Spong CY, Berghella V, Wenstrom KD, Mercer BM, Saade GR. Preventing the first cesarean delivery: summary of a joint Eunice Kennedy Shriver National Institute of Child Health and Human Development, Society for Maternal-Fetal Medicine, and American College of Obstetricians and Gynecologists Workshop. Obstet Gynecol. (2012) 120:1181–93. 10.1097/AOG.0b013e3182704880
    1. Lindsley DB. Heart and brain potentials of human fetuses in utero. By Donald B. Lindsley, 1942. Am J Psychol. (1987) 100:641–6. 10.2307/1422698
    1. Rosen MG, Scibetta JJ, Hochberg CJ. Fetal electroencephalography. IV. The FEEG during spontaneous and forceps births. Obstet Gynecol. (1973) 42:283–9.
    1. Eswaran H, Wilson JD, Lowery CL, Sharp G, Hawk RM, Murphy P, Pennington S. Brain stem auditory evoked potentials in the human fetus during labor. Am J Obstet Gynecol. (1999) 180:1422–6. 10.1016/S0002-9378(99)70029-3
    1. Thaler I, Boldes R, Timor-Tritsch I. Real-time spectral analysis of the fetal EEG: a new approach to monitoring sleep states and fetal condition during labor. Pediatr Res. (2000) 48:340–5. 10.1203/00006450-200009000-00013
    1. Howick J, Chalmers I, Glasziou P, Greenhalgh T, Heneghan C, Liberati A, Moschetti I, et al. OCEBM levels of evidence working group. The Oxford 2011 Levels of Evidence. (2011).
    1. Weller C, Dyson RJ, McFadyen IR, Green HL, Arias E. Fetal electroencephalography using a new, flexible electrode. Br J Obstet Gynaecol. (1981) 88:983–6. 10.1111/j.1471-0528.1981.tb01685.x
    1. Perinatologie/Geburtshilfe [Perinatology; obstetrics] Gynakol Rundsch. (1981) 21 Suppl 3:55–78. 10.1159/000269579
    1. Wilson PC, Philpott RH, Spies S, Ahmed Y, Kadichza M. The effect of fetal head compression and fetal acidaemia during labour on human fetal cerebral function as measured by the fetal electroencephalogram. Br J Obstet Gynaecol. (1979) 86:269–77. 10.1111/j.1471-0528.1979.tb11254.x
    1. Chik L, Sokol RJ, Rosen MG, Pillay SK, Jarrell SE. Trend analysis of intrapartum monitoring data: a basis for a computerized fetal monitor. Clin Obstet Gynecol. (1979) 22:665–79. 10.1097/00003081-197909000-00013
    1. Borgstedt AD, Heriot JT, Rosen MG, Lawrence RA, Sokol RJ. Fetal electroencephalography and one-minute and five-minute Apgar scores. J Am Med Womens Assoc. (1978) 33:220–2.
    1. Nemeadze NO. Effect of the untimely bursting of waters on the functional state of the fetus in labor. Akush Ginekol. (1978) 7:44–8.
    1. Chik L, Sokol RJ, Rosen MG, Regula GA, Borgstedt AD. Computer interpreted fetal monitoring data. Discriminant analysis or perinatal data as a model for prediction of neurologic status at one year of age. J Pediatr. (1977) 90:985–9. 10.1016/S0022-3476(77)80577-5
    1. Revol M, Challamel MJ, Fargier P, Bremond A, Chadenson O, Barrier PY. [An electroencephalographic study of the foetus during labour. Technique and interpretation (author's transl)]. Rev Electroencephalogr Neurophysiol Clin. (1977) 7:290–301. 10.1016/S0370-4475(77)80008-7
    1. Sokol RJ, Rosen MG, Chik L. Fetal electroencephalographic monitoring related to infant outcome. Am J Obstet Gynecol. (1977) 127:329–30. 10.1016/0002-9378(77)90481-1
    1. Chik L, Sokol RJ, Rosen MG, Borgstedt AD. Computer interpreted fetal electroencephalogram. I. Relative frequency of patterns. Am J Obstet Gynecol. (1976) 125:537–40. 10.1016/0002-9378(76)90373-2
    1. Chik L, Sokol RJ, Rosen MG, Borgstedt AD. Computer interpreted fetal electroencephalogram. II. Patterns in infants who were neurologically abnormal at 1 year of age. Am J Obstet Gynecol. (1976) 125:541–4. 10.1016/0002-9378(76)90374-4
    1. Hopp H, Beier R, Seidenschnur G, Heinrich J. [The significance of fetal electroencephalography for the diagnosis of fetal disorders]. Zentralbl Gynakol. (1976) 98:982–9.
    1. Borgstedt AD, Rosen MG, Chik L, Sokol RJ, Bachelder L, Leo P. Fetal electroencephalography. Relationship to neonatal and one-year developmental neurological examinations in high-risk infants. Am J Dis Child. (1975) 129:35–8. 10.1001/archpedi.1975.02120380021006
    1. Chik L, Rosen MG, Sokol RJ. An interactive computer program for studying fetal electroencephalograms. J Reprod Med. (1975) 14:154–8.
    1. Challamel MJ, Fargier P, Barrier PY, Revol M. [Fetal EEG during labor]. Rev Electroencephalogr Neurophysiol Clin. (1974) 4:429–33. 10.1016/S0370-4475(74)80053-5
    1. Fargier P, Bremond A, Challamel MJ, Barrier PY, Dolfus JM, Salomon B, Dargent D, Magnin P. L'électroencéphalogramme du fœtus au cours du travail et de l'accouchement. J Gynéc Obstét Biol Repr. (1974) 3:1023–33.
    1. Heinrich J, Seidenschnur G. [Methods and results of intranatal intensive care. II. The RFT-fetal monitor BMT 504]. Zentralbl Gynakol. (1974) 96:513–23.
    1. Beier R, Heinrich J, Hopp H, Seidenschnur G. [Problems in fetal electroencephalography]. Psychiatr Neurol Med Psychol. (1973) 25:92–7.
    1. Carretti N, Arfoudi A, Gaja R. [Fetal electroencephalographic changes during labor after administration of oxygen to the mother]. J Gynecol Obstet Biol Reprod. (1973) 2:79–86.
    1. Hopp H, Heinrich J, Seidenschnur G, Beier R. [Interpretation of simultaneously recorded fetal electroencephalograms and cardiotocograms]. Zentralbl Gynakol. (1973) 95:801–7.
    1. Peltzman P, Goldstein PJ, Battagin R. Quantitative analysis of fetal electrophysiologic data. Am J Obstet Gynecol. (1973) 115:1117–24. 10.1016/0002-9378(73)90562-0
    1. Peltzman P, Goldstein PJ, Battagin R. Optical analysis of the fetal electroencephalogram. Am J Obstet Gynecol. (1973) 116:957–62. 10.1016/S0002-9378(16)33843-1
    1. Rosen MG, Scibetta JJ, Hochberg CJ. Fetal electroencephalography. IV. The FEEG during spontaneous and forceps births. Obstet Gynecol. (1973) 42:283–9.
    1. Rosen MG, Scibetta J, Chik L, Borgstedt AD. An approach to the study of brain damage. The principles of fetal electroencephalography. Am J Obstet Gynecol. (1973) 115:37–47. 10.1016/0002-9378(73)90086-0
    1. Chachava KV, Devdariani MG, Zhordaniia ID, Loladze AS, Berulava AS. [Complex study of the mother and fetus in the 1st stage of physiological labor]. Akush Ginekol. (1972) 48:33–5.
    1. Hopp H, Heinrich J, Seidenschnur G, Beier R, Schultz H. [Preliminary results of fetal electroencephalography and cardiotocography]. Geburtshilfe Frauenheilkd. (1972) 32:629–34.
    1. Mann LI, Zwies A, Duchin S, Newman M. Human fetal electroencephalography: application of a vacuum electrode. Am J Obstet Gynecol. (1972) 114:898–903. 10.1016/0002-9378(72)90094-4
    1. Feldman JP, Le Houezec R, Sureau C. [Fetal electro-encephalography. Adjustment of an electrode allowing permanent recording during labor]. Gynecol Obstet. (1970) 69:491–3.
    1. Rosen MG, Scibetta JJ, Hochberg CJ. Human fetal electroencephalogram. 3. Pattern changes in presence of fetal heart rate alterations and after use of maternal medications. Obstet Gynecol. (1970) 36:132–40.
    1. Chachava KV, Devdariani MG, Loladze AS. [Several variants in the electroencephalogram of the fetus in normal and pathologic states]. Akush Ginekol. (1969) 45:18–21.
    1. Rosen MG, Scibetta JJ. The human fetal electroencephalogram. I. An electrode for continuous recording during labor. Am J Obstet Gynecol. (1969) 104:1057–60. 10.1016/0002-9378(69)90703-0
    1. Barden TP, Peltzman P, Graham JT. Human fetal electroencephalographic response to intrauterine acoustic signals. Am J Obstet Gynecol. (1968) 100:1128–34. 10.1016/S0002-9378(15)33414-1
    1. Rosen MG, Satran R. Fetal electroencephalography during birth. Obstet Gynecol. (1965) 26:740–5.
    1. De Haan HH, Gunn AJ, Williams CE, Gluckman PD. Brief repeated umbilical cord occlusions cause sustained cytotoxic cerebral edema and focal infarcts in near-term fetal lambs. Pediatr Res. (1997) 41:96–104. 10.1203/00006450-199701000-00015
    1. Thorngren-Jerneck K, Ley D, Hellström-Westas L, Hernandez-Andrade E, Lingman G, Ohlsson T, et al. . Reduced postnatal cerebral glucose metabolism measured by PET after asphyxia in near term fetal lambs. J Neurosci Res. (2001) 66:844–50. 10.1002/jnr.10051
    1. Kaneko M, White S, Homan J, Richardson B. Cerebral blood flow and metabolism in relation to electrocortical activity with severe umbilical cord occlusion in the near-term ovine fetus. Am J Obstet Gynecol. (2003) 188:961–72. 10.1067/mob.2003.219
    1. Gerrits LC, Battin MR, Bennet L, Gonzalez H, Gunn AJ. Epileptiform activity during rewarming from moderate cerebral hypothermia in the near-term fetal sheep. Pediatr Res. (2005) 57:342–6. 10.1203/01.PDR.0000150801.61188.5F
    1. Frasch MG, Keen AE, Gagnon R, Ross MG, Richardson BS. Monitoring fetal electrocortical activity during labour for predicting worsening acidemia: a prospective study in the ovine fetus near term. PLoS ONE. (2011) 6:e22100. 10.1371/journal.pone.0022100
    1. Wang X, Durosier LD, Ross MG, Richardson BS, Frasch MG. Online detection of fetal acidemia during labour by testing synchronization of EEG and heart rate: a prospective study in fetal sheep. PLoS ONE. (2014) 9:e108119. 10.1371/journal.pone.0108119
    1. Kurz CS, Miltner FO. [Dynamics of the fetal EEG spectral pattern in normal delivery (author's transl)]. Z Geburtshilfe Perinatol. (1980) 184:401–12.
    1. Bernstine RL, Borkowski WJ, Price AH. Prenatal fetal electroencephalography. Am J Obstet Gynecol. (1955) 70:623–30. 10.1016/0002-9378(55)90357-4
    1. Rosen MG, Scibetta JJ. The human fetal electroencephalogram. 2. Characterizing the EEG during labor. Neuropadiatrie. (1970) 2:17–26. 10.1055/s-0028-1091837
    1. Khopp K, Zaidenshnur G, Beier R, Kheinrikh I, Germann K. [Cardiotocographic and electroencephalographic studies in early diagnosis of fetal hypoxia]. Akush Ginekol. (1977) 10:27–31.
    1. Infant Collaborative Group Computerised interpretation of fetal heart rate during labour (INFANT): a randomised controlled trial. Lancet. (2017) 389:1719–29. 10.1016/S0140-6736(17)30568-8
    1. Huhmar E, Jaervinen PA. OBSERVATIONS ON FETAL ELECTROENCEPHALOGRAPHY. Ann Chir Gynaecol Fenn. (1963) 52:372–5.
    1. Frasch MG, Durosier LD, Gold N, Cao M, Matushewski B, Keenliside L, et al. . Adaptive shut-down of EEG activity predicts critical acidemia in the near-term ovine fetus. Physiol Rep. (2015) 3:e12435. 10.14814/phy2.12435
    1. Chik L, Sokol RJ, Rosen MG. Computer interpreted fetal electroencephalogram: sharp wave detection and classification of infants for one year neurological outcome. Electroencephalogr Clin Neurophysiol. (1977) 42:745–53. 10.1016/0013-4694(77)90227-9
    1. Morrison JL, Berry MJ, Botting KJ, Darby JRT, Frasch MG, Gatford KL, et al. . Improving pregnancy outcomes in humans through studies in sheep. Am J Physiol. (2018) 315:R1123–53. 10.1152/ajpregu.00391.2017
    1. Back SA, Riddle A, Dean J, Hohimer AR. The instrumented fetal sheep as a model of cerebral white matter injury in the premature infant. Neurotherapeutics. (2012) 9:359–70. 10.1007/s13311-012-0108-y
    1. Pryds O. Control of cerebral circulation in the high-risk Neonate. Ann Neurol. (1991) 30:321–29. 10.1002/ana.410300302
    1. Menke J, Michel E, Hillebrand S, Von Twickel J. Cross-spectral analysis of cerebral autoregulation dynamics in high risk preterm infants during the perinatal Period1. Pediatric. (1997) 10.1203/00006450-199711000-00023
    1. du Plessis AJ. Cerebrovascular injury in premature infants: current understanding and challenges for future prevention. Clin Perinatol. (2008) 35:609–41. 10.1016/j.clp.2008.07.010
    1. Soul JS, Hammer PE, Tsuji M, Saul JP, Bassan H, Limperopoulos C, et al. . Fluctuating pressure-passivity is common in the cerebral circulation of sick premature infants. Pediatr Res. (2007) 61:467–73. 10.1203/pdr.0b013e31803237f6
    1. Szymonowicz W, Walker AM, Yu VY, Stewart ML, Cannata J, Cussen L. Regional cerebral blood flow after hemorrhagic hypotension in the preterm, near-term, and newborn lamb. Pediatr Res. (1990) 28:361–6. 10.1203/00006450-199010000-00012
    1. Papile LA, Rudolph AM, Heymann MA. Autoregulation of cerebral blood flow in the preterm fetal lamb. Pediatr Res. (1985) 19:159–61. 10.1203/00006450-198502000-00001
    1. Tweed WA, Cote J, Pash M, Lou H. Arterial oxygenation determines autoregulation of cerebral blood flow in the fetal lamb. Pediatr Res. (1983) 17:246–9. 10.1203/00006450-198304000-00002
    1. Helou S, Koehler RC, Gleason CA, Jones MD, Jr, Traystman RJ. Cerebrovascular autoregulation during fetal development in sheep. Am J Physiol. (1994) 266:H1069–74. 10.1152/ajpheart.1994.266.3.H1069
    1. Hohimer AR, Bissonnette JM. Effects of cephalic hypotension, hypertension, and barbiturates on fetal cerebral blood flow and metabolism. Am J Obstet Gynecol. (1989) 161:1344–51. 10.1016/0002-9378(89)90695-9
    1. Dhillon SK, Lear CA, Galinsky R, Wassink G, Davidson JO, Juul S, et al. . The fetus at the tipping point: modifying the outcome of fetal asphyxia. J Physiol. (2018) 596:5571–92. 10.1113/JP274949
    1. Gunn AJ, Maxwell L, De Haan HH, Bennet L, Williams CE, Gluckman PD, et al. . Delayed hypotension and subendocardial injury after repeated umbilical cord occlusion in near-term fetal lambs. Am J Obstet Gynecol. (2000) 183:1564–72. 10.1067/mob.2000.108084
    1. Safe Prevention of the Primary Cesarean Delivery - ACOG Available online at: (accessed May 24, 2018).
    1. Yumoto Y, Satoh S, Fujita Y, Koga T, Kinukawa N, Nakano H. Noninvasive measurement of isovolumetric contraction time during hypoxemia and acidemia: fetal lamb validation as an index of cardiac contractility. Early Hum Dev. (2005) 81:635–42. 10.1016/j.earlhumdev.2005.04.004
    1. Astrup J. Energy-requiring cell functions in the ischemic brain. Their critical supply and possible inhibition in protective therapy. J Neurosurg. (1982) 56:482–97. 10.3171/jns.1982.56.4.0482
    1. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab. (2001) 21:1133–45. 10.1097/00004647-200110000-00001
    1. Rosen MG, Scibetta J. Documenting the human fetal EEG during birth. Electroencephalogr Clin Neurophysiol. (1969) 27:661. 10.1016/0013-4694(69)91233-4
    1. Resolution NHS. The Early Notification Scheme Progress Report: Collaboration and Improved Experience for Families. Sep 2019. Available online at:
    1. Paradise JL, Campbell TF, Dollaghan CA, Feldman HM, Bernard BS, Colborn DK, et al. . Receptive vocabulary and cognition in 3-year-old children in relation to otitis media in their first 3 years of life. Pediatr Res. (1997) 41:96. 10.1203/00006450-199704001-00584
    1. Okamoto Y, Kirikae. Electroencephalographic studies on brain of foetus, of children of premature birth and new-born, together with a note on reactions of foetus brain upon drugs. Folia Psychiatr Neurol Jpn. (1951) 5:135–46. 10.1111/j.1440-1819.1951.tb00583.x
    1. Blum T, Saling E, Bauer R. First magnetoencephalographic recordings of the brain activity of a human fetus. Br J Obstet Gynaecol. (1985) 92:1224–9. 10.1111/j.1471-0528.1985.tb04866.x
    1. Preissl H, Lowery CL, Eswaran H. Fetal magnetoencephalography: current progress and trends. Exp Neurol. (2004) 190 Suppl 1:S28–36. 10.1016/j.expneurol.2004.06.016
    1. Eswaran H, Haddad NI, Shihabuddin BS, Preissl H, Siegel ER, Murphy P, et al. . Non-invasive detection and identification of brain activity patterns in the developing fetus. Clin Neurophysiol. (2007) 118:1940–6. 10.1016/j.clinph.2007.05.072
    1. Haddad N, Govindan RB, Vairavan S, Siegel E, Temple J, Preissl H, et al. . Correlation between fetal brain activity patterns and behavioral states: an exploratory fetal magnetoencephalography study. Exp Neurol. (2011) 228:200–5. 10.1016/j.expneurol.2011.01.003
    1. Keen AE, Frasch MG, Sheehan MA, Matushewski B, Richardson BS. Maturational changes and effects of chronic hypoxemia on electrocortical activity in the ovine fetus. Brain Res. (2011) 1402:38–45. 10.1016/j.brainres.2011.05.043
    1. Keen AE, Frasch MG, Sheehan MA, Matushewski BJ, Richardson BS. Electrocortical activity in the near-term ovine fetus: automated analysis using amplitude frequency components. Brain Res. (2011) 1402:30–7. 10.1016/j.brainres.2011.05.044
    1. Rao N, Keen A, Czikk M, Frasch M, Richardson BS. Behavioural state linkage in the ovine fetus near term. Brain Res. (2009) 1250:149–56. 10.1016/j.brainres.2008.11.003

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