Abstract
Objective
To assess fetal behavioral changes in response to vibroacoustic stimulation (VAS) in normal singleton pregnancies using four-dimensional (4D) ultrasound.
Methods
Ten types of fetal movements and facial expressions in 68 healthy pregnant women between 24 and 40 weeks were studied using 4D ultrasound for 3 min before and after 3-s VAS. The frequencies of mouthing, yawning, tongue expulsion, back arch, jerky arm movement, startle movement, smiling, scowling, hand-to-face movement, and blinking were evaluated. The fetuses were subdivided into four gestational age groups (24–27, 28–31, 32–35, and ≥36 weeks). Comparison of the frequencies of the fetal behaviors before and after the stimulation in each gestational age group was conducted to detect the response to stimulation with advancing gestation.
Results
There were no significant differences in the frequency of each fetal behavior before and after VAS at 24–27, 28–31, and 32–35 weeks of gestation. However, the frequencies of blinking and startle movements were significantly higher after VAS in the 36–40 gestational age group (P < 0.05).
Conclusion
The age of 36 weeks of gestation might represent an advanced stage of brain and central nervous system development and maturation as the response to stimuli is prominent at this age compared with earlier gestation.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. Spencer JAD, Deans A, Nicolaidis P, Arulkumaran S. Fetal heart rate response to vibroacoustic stimulation during low and high heart rate variability episodes in late pregnancy. Am J Obstet Gynecol 1991;165:86–90.10.1016/0002-9378(91)90230-OSuche in Google Scholar
2. D’Elia A, Pighetti M, Vanacore F, Fabbrocini G, Arpaia L. Vibroacoustic stimulation in normal term human pregnancy. Early Hum Dev 2005;81:449–53.10.1016/j.earlhumdev.2004.04.017Suche in Google Scholar
3. Umstad M, Bailey C, Permezel M. Intrapartum fetal stimulation testing. Aust N Z J Obstet Gynaecol 1992;32:222–4.10.1111/j.1479-828X.1992.tb01951.xSuche in Google Scholar
4. East CE, Smyth R, Leader LR, Henshall NE, Colditz PB, Tan KH. Vibroacoustic stimulation for fetal assessment in labour in the presence of a nonreassuring fetal heart rate trace. Cochrane Database Syst Rev 2005;Article ID CD004664.10.1002/14651858.CD004664.pub2Suche in Google Scholar
5. Arulkumaran S, Talbert D, Hsu TS, Chua S, Anandakumar C, Ratnam SS. In-utero sound levels when vibroacoustic stimulation is applied to the maternal abdomen: an assessment of the possibility of cochlea damage in the fetus. Br J Obstet Gynaecol 1992;99:43–5.10.1111/j.1471-0528.1992.tb14390.xSuche in Google Scholar
6. Arulkumaran S, Skurr B, Tong H, Kek LP, Yeoh KH, Ratnam SS. No evidence of hearing loss due to fetal acoustic stimulation test. Obstet Gynecol 1991;78:283–5.Suche in Google Scholar
7. Visser GHA, Mulder HH, Wit HP, Mulder EJH, Prechtl HFR.Vibro-acoustic stimulation of the human fetus: effect on behavioural state organization. Early Hum Dev 1989;19:285–96.10.1016/0378-3782(89)90063-7Suche in Google Scholar
8. Nijhuis JG, Prechtl HFR, Martin CB Jr, Bots RS. Are there behavioral states in the human fetus? Early Hum Dev 1982;6:177–95.10.1016/0378-3782(82)90106-2Suche in Google Scholar
9. Horimoto N, Koyanagi T, Maeda H, Satoh S, Takashima T, Minami T, et al. Can brain impairment be detected by in utero behavioural patterns? Arch Dis Child 1993;69:3–8.10.1136/adc.69.1_Spec_No.3Suche in Google Scholar
10. Prechtl HFR, Einspieler C. Is neurological assessment of the fetus possible? Eur J Obstet Gynecol Reprod Biol 1997;75:81–4.10.1016/S0301-2115(97)00197-8Suche in Google Scholar
11. Kurjak A, Andonotopo W, Hafner T, Salihagic-Kadic A, Stanojevic M, Azumeni G, et al. Normal standards for fetal neurobehavioral developments – longitudinal quantification by four-dimensional sonography. J Perinat Med 2006;34:56–65.10.1515/JPM.2006.007Suche in Google Scholar PubMed
12. Hata T, Dai SY, Marumo G. Ultrasound for evaluation of fetal neurobehavioral development: from 2-D to 4-D. Infant Child Dev 2010;19:99–118.10.1002/icd.659Suche in Google Scholar
13. Hata T, Kanenishi J, Hanoka U, Uematsu R, Marumo G, Tanaka H. HDlive study of fetal development and behavior. Donald School J Ultrasound Obstet Gynecol 2014;8:250–65.10.5005/jp-journals-10009-1363Suche in Google Scholar
14. Sajapala S, AboEllail MAM, Kanenishi K, Mori N, Marumo G, Hata T. 4D ultrasound study of fetal movement early in the second trimester of pregnancy. J Perinat Med 2017;45:737–43.10.1515/jpm-2016-0250Suche in Google Scholar
15. AboEllail MAM, Hata T. Fetal face as important indicator of fetal brain function. J Perinat Med 2017;45:729–36.10.1515/jpm-2016-0377Suche in Google Scholar
16. Hata T, Kanenishi K, Sasaki M, Yanagihara T. Fetal reflex movement in twin pregnancies late in the first trimester: 4-D sonographic study. Ultrasound Med Biol 2011;237:1948–51.10.1016/j.ultrasmedbio.2011.06.005Suche in Google Scholar
17. AboEllail MAM, Kanenishi K, Mori N, Mohamed OAK, Hata T. 4D ultrasound study of fetal facial expressions in the third trimester of pregnancy. J Matern Fetal Neonatal Med 2018;31:1856–64.10.1080/14767058.2017.1330880Suche in Google Scholar
18. Morokuma S, Fukushima K, Kawai N, Tomonaga M, Satoh S, Nakano H. Fetal habituation correlates with functional brain development. Behav Brain Res 2004;153:459–63.10.1016/j.bbr.2004.01.002Suche in Google Scholar
19. van Heteren CF, Boekkooi PF, Schiphorst RH, Jongsma HW, Nijhuis JG. Fetal habituation to vibroacoustic stimulation in uncomplicated postterm pregnancies. Eur J Obstet Gynecol Reprod Biol 2001;97:178–82.10.1016/S0301-2115(00)00543-1Suche in Google Scholar
20. Gerhardt KJ, Abrams RM. Fetal exposure to sound and vibroacoustic stimulation. J Perinatol 2000;20:S21–30.10.1038/sj.jp.7200446Suche in Google Scholar PubMed
21. Fox HE, Badalian SS. Fetal movement in response to vibroacuostic stimulation: a review. Obstet Gynecol Surv 1993;48:707–13.10.1097/00006254-199310000-00027Suche in Google Scholar PubMed
22. Groome LJ, Bentz LS, Singh KP, Mooney DM. Behavioral state change in normal human fetuses following a single vibroacoustic stimulus: effect of duration of quiet sleep prior to stimulation. Early Hum Dev 1993;33:21–7.10.1016/0378-3782(93)90170-YSuche in Google Scholar
23. Pietrantoni M, Angel JL, Parsons MT, McClain L, Arango HA, Spellacy WN. Human fetal response to vibroacoustic stimulation as a function of stimulus duration. Obstet Gynecol 1991;87:807–11.Suche in Google Scholar
24. Devoe L. Vibroacoustic stimuli and fetal behavior. Nurs Times 1991;87:36–7.Suche in Google Scholar
25. Sadovsky E, Ohel G, Simon A. Ultrasonographical evaluation of the incidence of simultaneous and independent movements in twin fetuses. Gynecol Obstet Invest 1987;23:5–9.10.1159/000298826Suche in Google Scholar
26. Tan KH, Smyth RM, Wei X. Fetal vibroacoustic stimulation for facilitation of tests of fetal wellbeing. Cochrane Database Syst Rev 2013;12:CD002963.10.1002/14651858.CD002963Suche in Google Scholar
27. DiPietro JA, Hodgson DM, Costigan KA, Johnson TR. Fetal antecedents of infant temperament. Child Dev 1996;67:2568–83.10.2307/1131641Suche in Google Scholar
28. Kawai N, Morokuma S, Tomonaga M, Horimoto N, Tanada M. Associative learning and memory in a chimpanzee fetus: learning and long-lasting memory before birth. Dev Psychobiol 2004;44:116–22.10.1002/dev.10160Suche in Google Scholar
29. Makino I, Matsuda Y, Yoneyama M, Hirasawa K, Takagi K, Ohta H, et al. Effect of maternal stress on fetal heart rate assessed by vibroacoustic stimulation. J Int Med Res 2009;37:1780–8.10.1177/147323000903700614Suche in Google Scholar
30. Kiuchi M, Nagata N, Ikeno S, Terakawa N. The relationship between the response to external light stimulation and behavioral states in the human fetus: how it differs from vibroacoustic stimulation. Early Hum Dev 2000;58:153–65.10.1016/S0378-3782(00)00074-8Suche in Google Scholar
31. Hata T, Kanenishi K, AboEllail MAM, Marumo G, Kurjak A. Fetal consciousness: four-dimensional ultrasound study. Donald School J Ultrasound Obstet Gynecol 2015;9:471–4.10.5005/jp-journals-10009-1434Suche in Google Scholar
32. Reissland N, Francis B, Mason J. Can healthy fetuses show facial expressions of “pain” or “distress”? PLoS One 2013;8:e65530.10.1371/journal.pone.0065530Suche in Google Scholar PubMed PubMed Central
33. Marx V, Nagy E. Fetal behavioural responses to maternal voice and touch. PLoS One 2015;10:e0129118.10.1371/journal.pone.0129118Suche in Google Scholar PubMed PubMed Central
34. Kiuchi M, Nagata N, Ikeno S, Terakawa N. The relationship between the response to external light stimulation and behavioral states in the human fetus: how it differs from vibroacoustic stimulation. Early Hum Dev 2000;58:153–65.10.1016/S0378-3782(00)00074-8Suche in Google Scholar
35. Lopez-Teijon M, Garcia-Faura A, Prats-Galino A. Fetal facial expression in response to intravaginal music emission.Ultrasound 2015;23:216–23.10.1177/1742271X15609367Suche in Google Scholar
36. Gangon R, Hunse C, Carmichael L, Fellows F, Patrick J. Human fetal response to vibratory acoustic stimulation from twenty-six weeks to term. Am J Obstset Gynecol 1987;157:1375–81.10.1016/S0002-9378(87)80227-2Suche in Google Scholar
37. Crade M, Lovett S. Fetal response to sound stimulation: preliminary report exploring use of sound stimulation in routine obstetrical ultrasound examinations. J Ultrasound Med 1988;7:499–503.10.7863/jum.1988.7.9.499Suche in Google Scholar
38. Luz SH, Vasconcellos FC, Kreling T, Pacheco FS, Chaves ML. Evaluation of normal neurological development of human fetuses from 21 to 30 weeks’ gestation through fetal auditory evoked response. J Perinat Med 2009;37:270–5.10.1515/JPM.2009.048Suche in Google Scholar
39. Divon MY, Platt LD, Cantrell CJ, Smith CV, Yeh Sze YA, Paul RH. Evoked fetal startle response: a possible intrauterine neurological examination. Am J Obstet Gynecol 1985;153:454–6.10.1016/0002-9378(85)90086-9Suche in Google Scholar
40. Blumenthal TD, Goode CT. The startle eyeblink response to low intensity acoustic stimuli. Psychophysiology 1991;28: 296–306.10.1111/j.1469-8986.1991.tb02198.xSuche in Google Scholar PubMed
41. Valls-Solé J. Assessment of excitability in brainstem circuits mediating the blink reflex and the startle reaction. Clin Neurophysiol 2012;123:13–20.10.1016/j.clinph.2011.04.029Suche in Google Scholar PubMed
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/jpm-2018-0344).
©2019 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Editorial
- Preterm premature rupture of membranes (PPROM)
- Original Articles – Obstetrics
- The value of amniotic fluid analysis in patients with suspected clinical chorioamnionitis
- Patients with acute cervical insufficiency without intra-amniotic infection/inflammation treated with cerclage have a good prognosis
- Maternal serum endocan concentrations are elevated in patients with preterm premature rupture of membranes
- The earlier the gestational age, the greater the intensity of the intra-amniotic inflammatory response in women with preterm premature rupture of membranes and amniotic fluid infection by Ureaplasma species
- Assessment of maternal GBS colonization and early-onset neonatal disease rate for term deliveries: a decade perspective
- Clinical importance of the 75-g glucose tolerance test (GTT) in the prediction of large for gestational age (LGA) fetuses in non-diabetic pregnancies
- Expression of genes involved in inflammation and growth – does sampling site in human full-term placenta matter?
- Impact of cell-free fetal DNA on invasive prenatal diagnostic tests in a real-world public setting
- Perinatal outcome in gestational diabetes according to different diagnostic criteria
- Original Articles – Fetus
- Change in fetal behavior in response to vibroacoustic stimulation
- Diagnostic accuracy of isolated clubfoot in twin compared to singleton gestations
- Original Article – Newborn
- Usefulness of transcutaneous bilirubin assessment measured in non-photo-exposed skin to guide the length of phototherapy: an observational study
- Letters to the Editor
- Methodological issues on the clinical importance of the 75-g glucose tolerance test (GTT) in the prediction of large for gestational age (LGA) fetuses in non-diabetic pregnancies
- Reply to the Letter to the Editor: methodological issues on the clinical importance of the 75-g glucose tolerance test (GTT) in the prediction of large-for-gestational-age (LGA) fetuses in non-diabetic pregnancies
Artikel in diesem Heft
- Frontmatter
- Editorial
- Preterm premature rupture of membranes (PPROM)
- Original Articles – Obstetrics
- The value of amniotic fluid analysis in patients with suspected clinical chorioamnionitis
- Patients with acute cervical insufficiency without intra-amniotic infection/inflammation treated with cerclage have a good prognosis
- Maternal serum endocan concentrations are elevated in patients with preterm premature rupture of membranes
- The earlier the gestational age, the greater the intensity of the intra-amniotic inflammatory response in women with preterm premature rupture of membranes and amniotic fluid infection by Ureaplasma species
- Assessment of maternal GBS colonization and early-onset neonatal disease rate for term deliveries: a decade perspective
- Clinical importance of the 75-g glucose tolerance test (GTT) in the prediction of large for gestational age (LGA) fetuses in non-diabetic pregnancies
- Expression of genes involved in inflammation and growth – does sampling site in human full-term placenta matter?
- Impact of cell-free fetal DNA on invasive prenatal diagnostic tests in a real-world public setting
- Perinatal outcome in gestational diabetes according to different diagnostic criteria
- Original Articles – Fetus
- Change in fetal behavior in response to vibroacoustic stimulation
- Diagnostic accuracy of isolated clubfoot in twin compared to singleton gestations
- Original Article – Newborn
- Usefulness of transcutaneous bilirubin assessment measured in non-photo-exposed skin to guide the length of phototherapy: an observational study
- Letters to the Editor
- Methodological issues on the clinical importance of the 75-g glucose tolerance test (GTT) in the prediction of large for gestational age (LGA) fetuses in non-diabetic pregnancies
- Reply to the Letter to the Editor: methodological issues on the clinical importance of the 75-g glucose tolerance test (GTT) in the prediction of large-for-gestational-age (LGA) fetuses in non-diabetic pregnancies