Nonlinear analysis of fetal heart rate dynamics in fetuses compromised by asymptomatic partial placental abruption
Open accessAbstract
Introduction We analyzed fetal heart rate (FHR) parameters, dynamics, and outcomes in pregnancies with asymptomatic partial placental abruption (PPA) compared with those in normal pregnancies.Methods We examined nonstress test (NST) data acquired from 2003 to 2012 at our institution. Normal pregnancies (N = 170) and PPA cases (N = 17) were matched for gestational age, fetal sex, and mean FHR. NSTs were performed at 33-42 weeks of gestation. FHR parameters obtained from the NST and perinatal outcomes were analyzed using linear methods. Nonlinear indices, including approximate entropy (ApEn), sample entropy (SampEn), short-term and long-term scaling exponents (α1 and α2), and correlation dimension (CD), were used to interpret FHR dynamics and system complexity. The area under a receiver operating characteristic curve (AUC) was used to evaluate the nonlinear indices.Results There were no significant differences in general characteristics and FHR parameters between the PPA and control groups. However, gestational age at delivery, birth weight, 5-min Apgar scores, ApEn, SampEn, and CD were significantly lower in the PPA group than in the control group (P < 0.05). The long-term scaling exponent (α2) and crossover index (α2/α1) of the PPA fetuses were significantly higher than those of the controls (P < 0.01). A multiple regression model showed better performance in predicting PPA (AUC, 0.92; sensitivity 82.35%; specificity, 94.12%).Discussion Nonlinear dynamic indices of FHR in asymptomatic PPA were qualitatively different from those in normal pregnancies, whereas the conventional FHR parameters were not significantly different.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Several studies suggest that acute abruption is a significant contributor to category III fetal heart rate patterns due to terminal bradycardia and sinusoidal fetal heart rate patterns.
“Several studies suggest that acute abruption is a significant contributor to category III FHR patterns due to terminal bradycardia and sinusoidal FHR patterns (62, 64–68).”
From Placental abruption at near-term and term gestations: Pathophysiology, epidemiology, diagnosis, and management (2023) · cites this paper as [65]
A wide array of abnormal fetal heart rate patterns is possible in abruption, reflecting the underlying pathophysiology of this condition.
“A wide array of abnormal FHR patterns is possible (62–65), reflecting the underlying pathophysiology of this condition (TABLE 3).”
From Placental abruption at near-term and term gestations: Pathophysiology, epidemiology, diagnosis, and management (2023) · cites this paper as [65]
Cites
Physiological time-series analysis using approximate entropy and sample entropy
Richman, J. S., & Moorman, J. R. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.278.6.h2039 · Cited by 7,880 · see citing works
Measuring the strangeness of strange attractors
Grassberger, P., & Procaccia, I. (1983) · Physica D Nonlinear Phenomena · doi:10.1016/0167-2789(83)90298-1 · Cited by 5,697 · see citing works
Independent coordinates for strange attractors from mutual information
Fraser, A. M., & Swinney, H. L. (1986) · Physical Review A · doi:10.1103/physreva.33.1134 · Cited by 4,637 · see citing works
Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series
Peng, C., Havlin, S., Stanley, E., & Goldberger, A. L. (1995) · Chaos An Interdisciplinary Journal of Nonlinear Science · doi:10.1063/1.166141 · Cited by 3,865 · see citing works
Loss of 'Complexity' and Aging
Lipsitz, L. A. (1992) · JAMA · doi:10.1001/jama.1992.03480130122036 · Cited by 1,268 · see citing works
Non-linear dynamics for clinicians: chaos theory, fractals, and complexity at the bedside
Goldberger, A. L. (1996) · The Lancet · doi:10.1016/s0140-6736(96)90948-4 · Cited by 859 · see citing works
Age-related alterations in the fractal scaling of cardiac interbeat interval dynamics
Iyengar, N., Peng, C., Morin, R. J., Goldberger, A. L., & Lipsitz, L. A. (1996) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1996.271.4.r1078 · Cited by 703 · see citing works
Ho, K. K. L., Moody, G. B., Peng, C.-K., Mietus, J. E., Larson, M. G., Levy, D., & Goldberger, A. L. (1997) · Circulation · doi:10.1161/01.cir.96.3.842 · Cited by 489 · see citing works
Approximate entropy: a regularity measure for fetal heart rate analysis.
Pincus, S. M., & Viscarello, R. R. (1992) · PubMed · Cited by 323 · see citing works
Clinical presentation and risk factors of placental abruption
Tikkanen, M., Nuutila, M., Hiilesmaa, V., Paavonen, J., & Ylikorkala, O. (2006) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1080/00016340500449915 · Cited by 186 · see citing works
Intrapartum fetal heart rate monitoring
Krebs, H. B., Petres, R. E., Dunn, L. J., Jordaan, H. V. F., & Segreti, A. C. (1980) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(16)32835-6 · Cited by 165 · see citing works
PIPER, J., Xenakis, E. M.-J., MCFARLAND, M., ELLIOTT, B., Berkus, M. D., & Langer, O. (1996) · Obstetrics and Gynecology · doi:10.1016/0029-7844(95)00400-9 · Cited by 160 · see citing works
The syndrome of chronic abruptio placentae, hydrorrhea, and circumvallate placenta
Naftolin, F. N., Khudr, G., Benirschke, K., & Hutchinson, D. L. (1973) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)31292-8 · Cited by 111 · see citing works
Intrapartum fetal heart rate monitoring
Krebs, H. B., Petres, R. E., & Dunn, L. J. (1983) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(83)90714-7 · Cited by 93 · see citing works
Computerized analysis of fetal heart rate parameters by gestational age
Park, M., Hwang, J. H., Cha, K. J., Park, Y. S., & Koh, S. (2001) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(01)00423-4 · Cited by 46 · see citing works
Li, X., Zheng, D.-A., Zhou, S., Tang, D., Wang, C., & Wu, G. (2005) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/j.0001-6349.2005.00773.x · Cited by 40 · see citing works
Fetal heart rate pattern reflecting the severity of placental abruption
Usui, R., Matsubara, S., Ohkuchi, A., Kuwata, T., Watanabe, T., Izumi, A., & Suzuki, M. (2008) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-007-0471-9 · Cited by 35 · see citing works
Alterations in irregular and fractal heart rate behavior in growth restricted fetuses
Yum, M., Park, E., Kim, C., & Hwang, J.-H. (2001) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00314-6 · Cited by 27 · see citing works
Fractal analysis: a new method for evaluating fetal heart rate variability
Renzo, G. C. D., Montani, M., Fioriti, V. A., Clerici, G., Branconi, F., Pardini, A., Indraccolo, S. R., & Cosmi, E. V. (1996) · Journal of Perinatal Medicine · doi:10.1515/jpme.1996.24.3.261 · Cited by 25 · see citing works
Detrended fluctuation analysis: a suitable method for studying fetal heart rate variability?
Echeverría, J. C., Hayes‐Gill, B., Crowe, J. A., Woolfson, M. S., & Croaker, G. D. H. (2004) · Physiological Measurement · doi:10.1088/0967-3334/25/3/015 · Cited by 25 · see citing works
Fetal heart rate patterns related to neonatal brain damage and neonatal death in placental abruption
Takano, Y., Furukawa, S., Ohashi, M., Michikata, K., Sameshima, H., & Ikenoue, T. (2013) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2012.01945.x · Cited by 20 · see citing works
Detrended Fluctuation Analysis of Heart Rate Variability in Normal and Growth-Restricted Fetuses
Kikuchi, A., Unno, N., Kōzuma, S., & Taketani, Y. (2007) · Gynecologic and Obstetric Investigation · doi:10.1159/000109266 · Cited by 19 · see citing works
Chaotic indices and canonical ensemble of heart rate patterns in small-for-gestational age fetuses
Hoh, J., Park, Y.-S., Cha, K.-J., Oh, J.-E., Lee, H.-J., Lee, G.-T., & Park, M.-I. (2007) · Journal of Perinatal Medicine · doi:10.1515/jpm.2007.044 · Cited by 16 · see citing works
Park, Y.-S., Ryu, K., Shim, S. S., Hoh, J., & Park, M.-I. (2012) · Early Human Development · doi:10.1016/j.earlhumdev.2012.08.006 · Cited by 12 · see citing works
Park, Y.-S., Hoh, J., Koh, S., Shin, J., & Park, M.-I. (2010) · Fetal Diagnosis and Therapy · doi:10.1159/000314907 · Cited by 5 · see citing works
Intrapartum fetal heart rate monitoring
T. Ikeda, H. S. (2006) · CRC Press eBooks · doi:10.3109/9781439814697-161 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Brandt, J. S., & Ananth, C. V. (2023) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2022.06.059 · Cited by 115 · see citing works
Mayor, D. F., Panday, D., Kandel, H. K., Steffert, T., & Banks, D. (2021) · Entropy · doi:10.3390/e23030321 · Cited by 40 · see citing works
Saleem, S., Naqvi, S. S., Manzoor, T., Saeed, A., Rehman, N. U., & Mirza, J. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00246 · Cited by 36 · see citing works
Non-linear Methods Predominant in Fetal Heart Rate Analysis: A Systematic Review
Ribeiro, M., Monteiro-Santos, J., Castro, L., Antunes, L. F., Santos, C., Teixeira, A., & Henriques, T. S. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.661226 · Cited by 22 · see citing works
Cuesta–Frau, D., Novák, D., Burda, V., Molina, Á., Vargas, B., Mráz, M., Kaválková, P., Beneš, M., & Haluzı́k, M. (2018) · Entropy · doi:10.3390/e20110871 · Cited by 14 · see citing works
Complexity analysis of fetal heart rate preceding intrauterine demise
Schnettler, W. T., Goldberger, A. L., Ralston, S. J., & Costa, M. D. (2016) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2016.06.025 · Cited by 7 · see citing works
Diagnosis of placental abruption: a legal issue for physicians
Saccone, G., Maruotti, G. M., Paternoster, M., & Martinelli, P. (2016) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2016.1153061 · Cited by 5 · see citing works
Significance of Clinical Findings of Patients with Placental Abruption
Jeong, Y. Y., Yun, T. H., Hong, S. Y., & Bae, J. Y. (2020) · Perinatology · doi:10.14734/pn.2020.31.3.123 · Cited by 2 · see citing works
Imputation Method for Fetal Heart Rate Signal Evaluation Based on Optimal Transport Theory
Wang, C., Long, S., Zeng, R., & Lu, Y. (2021) · SN Computer Science · doi:10.1007/s42979-021-00805-3 · Cited by 3 · see citing works
Park, Y.-S., Choi, E., Ryu, K., & Hoh, J. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4197927
Observer-based saturated impulsive control for nonlinear systems
Zhang, H. (2025) · International Conference on Applied Mathematics, Modelling and Intelligent Computing (CAMMIC) · doi:10.1145/3745533.3745652
Identification and Management of Presumed Intrapartum Fetal Distress
Rosser, S., Daly, M. E., Turner, J., & Kumar, S. (2025) · Cambridge University Press eBooks · doi:10.1017/9781009497459.007
- Authors
- Choi, W.-Y., & Hoh, J.-K.
- Affiliations
- Hanbat National University (KR)
- Hanyang University (KR)
- Corresponding author
- Hoh, Jeong-Kyu
- ORCID
- Hoh, Jeong-Kyu
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 2015-12
- Volume
- 36
- Issue
- 12
- Pages
- 1474-1479
- ISSN
- 0143-4004 (ISSN-L)
- OpenAlex
- W2180241589
- Cited by
- 12
- References
- 26
- Citations by year
- 2025: 2 · 2023: 1 · 2022: 1 · 2021: 3 · 2020: 1 · 2019: 1 · 2018: 1 · 2016: 2
- FWCI
- 0.73
- Type
- journal article
- Language
- en
- Open access
- Licence
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- The Royal Society of Chemistry’s Journals, Books and Databases (The Royal Society of Chemistry) (submittedVersion, cc-by-nc-nd)
- Funders
- Research Fund of Hanyang University (201200000000601)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Maternal and fetal healthcare
- Keywords
- nonlinear dynamics, approximate entropy, sample entropy, correlation dimension, scaling exponents, nonstress test, perinatal outcomes, fetal well-being
- MeSH terms
- Abruptio Placentae, Adult, Female, Gestational Age, Heart Rate, Fetal, Humans, Male, Pregnancy, Nonlinear Dynamics, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review