{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,29]],"date-time":"2026-05-29T13:41:17Z","timestamp":1780062077277,"version":"3.54.0"},"reference-count":36,"publisher":"Walter de Gruyter GmbH","issue":"4","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2017,5,24]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec id=\"j_jpm-2015-0275_s_999_w2aab3b7c18b1b6b1aab1c15b1Aa\"><jats:title>Objective:<\/jats:title><jats:p>The objective of this study is to investigate the alterations caused by smoking on the features of fetal heart rate (FHR) tracings as well as to make a comparison between pregnant smokers and pregnant women with intrauterine growth restriction (IUGR).<\/jats:p><\/jats:sec><jats:sec id=\"j_jpm-2015-0275_s_998_w2aab3b7c18b1b6b1aab1c15b2Aa\"><jats:title>Study design:<\/jats:title><jats:p>A number of established features derived from linear and nonlinear fields were employed to study the possible influence of maternal smoking on FHR tracings. Moreover, correlation and measures of complexity of the FHR were explored, in order to get closer to the core of information that the signal of FHR tracings conveys. Data included FHR tracings from 61 uncomplicated singleton pregnancies, 16 pregnant smoker cases, and 15 pregnancies of women with IUGR.<\/jats:p><\/jats:sec><jats:sec id=\"j_jpm-2015-0275_s_997_w2aab3b7c18b1b6b1aab1c15b3Aa\"><jats:title>Results:<\/jats:title><jats:p>The analysis of FHR indicated that some parameters, such as mutual information (P=0.0025), multiscale entropy (P=0.01), and algorithmic complexity (P=0.024) appeared decreased in the group of pregnant smokers, while kurtosis (P=0.0011) increased. The comparison between pregnant smokers and pregnant women with IUGR indicated a reduction in Hjorth complexity (P=0.039) for the former.<\/jats:p><\/jats:sec><jats:sec id=\"j_jpm-2015-0275_s_996_w2aab3b7c18b1b6b1aab1c15b4Aa\"><jats:title>Conclusion:<\/jats:title><jats:p>Smoking during pregnancy seems to induce differences in several linear and nonlinear indices in recordings of FHR tracings. This may be the consequence of an altered neurodevelopmental maturation possibly resulting from chronic fetal hypoxemia in cigarette-exposed fetuses.<\/jats:p><\/jats:sec>","DOI":"10.1515\/jpm-2015-0275","type":"journal-article","created":{"date-parts":[[2016,4,7]],"date-time":"2016-04-07T18:39:40Z","timestamp":1460054380000},"page":"403-411","source":"Crossref","is-referenced-by-count":8,"title":["The effect of cigarette smoking on fetal heart rate tracing during pregnancy"],"prefix":"10.1515","volume":"45","author":[{"given":"Kyriaki","family":"Spyridou","sequence":"first","affiliation":[{"name":"School of Medicine , Laboratory of Medical Informatics , Aristotle University of Thessaloniki , Plastira 1 , Thessaloniki 56535 , Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8915-6658","authenticated-orcid":false,"given":"Ioanna","family":"Chouvarda","sequence":"additional","affiliation":[{"name":"School of Medicine , Laboratory of Medical Informatics , Aristotle University of Thessaloniki , Thessaloniki , Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9932-9302","authenticated-orcid":false,"given":"Leontios","family":"Hadjileontiadis","sequence":"additional","affiliation":[{"name":"Department of Electrical and Computer Engineering , Polytechnic School , Aristotle University of Thessaloniki , Thessaloniki , Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nikolaos","family":"Maglaveras","sequence":"additional","affiliation":[{"name":"School of Medicine , Laboratory of Medical Informatics , Aristotle University of Thessaloniki , Thessaloniki , Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"374","published-online":{"date-parts":[[2016,4,7]]},"reference":[{"key":"2023040100110807885_j_jpm-2015-0275_ref_001_w2aab3b7c18b1b6b1ab2ab1Aa","doi-asserted-by":"crossref","unstructured":"Parer JT, King T. Fetal heart rate monitoring: is it salvageable? Am J Obstet Gynecol. 2000;182:982\u20137.","DOI":"10.1016\/S0002-9378(00)70358-9"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_002_w2aab3b7c18b1b6b1ab2ab2Aa","doi-asserted-by":"crossref","unstructured":"Signorini MG, Magenes G, Cerutti S, Arduini D. Linear and nonlinear parameters for the analysis of fetal heart rate signal from cardiotocographic recordings. IEEE Trans Biomed Eng. 2003;50:365\u201374.","DOI":"10.1109\/TBME.2003.808824"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_003_w2aab3b7c18b1b6b1ab2ab3Aa","doi-asserted-by":"crossref","unstructured":"Morrow R, Ritchie JW, Bull SB. Maternal cigarette smoking: the effects on umbilical and uterine blood flow velocity. Am J Obstet Gynecol. 1988;159:1069\u201371.","DOI":"10.1016\/0002-9378(88)90415-2"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_004_w2aab3b7c18b1b6b1ab2ab4Aa","doi-asserted-by":"crossref","unstructured":"Lambers DS, Clark KE. The maternal and fetal physiologic effects of nicotine. Semin Perinmatol. 1996;20:115\u201326.","DOI":"10.1016\/S0146-0005(96)80079-6"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_005_w2aab3b7c18b1b6b1ab2ab5Aa","doi-asserted-by":"crossref","unstructured":"Quigley ME, Sheehan KL, Wilkes MM, Yen SS. Effects of maternal smoking on circulating catecholamine levels and fetal heart rates. Am J Obstet Gynecol. 1979;133:685\u201390.","DOI":"10.1016\/0002-9378(79)90019-X"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_006_w2aab3b7c18b1b6b1ab2ab6Aa","doi-asserted-by":"crossref","unstructured":"Slotkin T. Fetal nicotine or cocaine exposure: which one is worse? J Pharmacol Exp Ther. 1998;285:931\u201345.","DOI":"10.1016\/S0022-3565(24)37495-6"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_007_w2aab3b7c18b1b6b1ab2ab7Aa","doi-asserted-by":"crossref","unstructured":"Windham GC, Von Behren J, Waller K, Fenster L. Exposure to environmental and mainstream tobacco smoke and risk of environmental and mainstream tobacco smoke and risk of spontaneous abortion. Am J Epidemiol. 1999;149:243\u20137.","DOI":"10.1093\/oxfordjournals.aje.a009798"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_008_w2aab3b7c18b1b6b1ab2ab8Aa","doi-asserted-by":"crossref","unstructured":"Lewis K, Bosque E. Deficient hypoxia awakening response in infants of smoking mothers: possible relationship to sudden infant death syndrome. J Pediatr. 1995;127:691\u20139.","DOI":"10.1016\/S0022-3476(95)70155-9"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_009_w2aab3b7c18b1b6b1ab2ab9Aa","doi-asserted-by":"crossref","unstructured":"Lurie S, Ribenzaft S, Boaz M, Golan A, Sadan O. The effect of cigarette smoking during pregnancy on mode of delivery in uncomplicated term singleton pregnancies. J Matern Fetal Neonatal Med. 2014;27:812\u20135.","DOI":"10.3109\/14767058.2013.842551"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_010_w2aab3b7c18b1b6b1ab2ac10Aa","doi-asserted-by":"crossref","unstructured":"Godfrey KM, Redman G, Barker DJP, Osmond C. The effect of maternal anaemia and iron deficiency on the ratio of fetal weight to placental weight. Br J Obstet Gynaecol. 1991;98:886\u201391.","DOI":"10.1111\/j.1471-0528.1991.tb13510.x"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_011_w2aab3b7c18b1b6b1ab2ac11Aa","doi-asserted-by":"crossref","unstructured":"Barker DJP. Fetal origins of coronary heart disease. Br Med J. 1995;311:171\u20134.","DOI":"10.1136\/bmj.311.6998.171"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_012_w2aab3b7c18b1b6b1ab2ac12Aa","doi-asserted-by":"crossref","unstructured":"ACOG practice bulletin. Intrauterine growth restriction. N12 January 2000. Int J Gynecol Obstet. 2001;72:85\u201396.","DOI":"10.1016\/S0020-7292(00)90000-6"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_013_w2aab3b7c18b1b6b1ab2ac13Aa","doi-asserted-by":"crossref","unstructured":"Gieratowski J, Hoyer D, Teschke F, Nowack S, Schneider U, Zebrowski J. Development of multiscale complexity and multifractality of fetal heart rate variability. Auton Neurosci. 2013;178:29\u201336.","DOI":"10.1016\/j.autneu.2013.01.009"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_014_w2aab3b7c18b1b6b1ab2ac14Aa","doi-asserted-by":"crossref","unstructured":"Kugiumtzis D, Tsimpiris A. Measures of analysis of time series (MATS): a matlab toolkit for computation of multiple measures on time series data bases. J Stat Softw. 2010;33:1\u201328.","DOI":"10.18637\/jss.v033.i05"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_015_w2aab3b7c18b1b6b1ab2ac15Aa","doi-asserted-by":"crossref","unstructured":"Latham PE, Roudi Y. Mutual information. Scholarpedia. 2009;4:1658.","DOI":"10.4249\/scholarpedia.1658"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_016_w2aab3b7c18b1b6b1ab2ac16Aa","doi-asserted-by":"crossref","unstructured":"Ho KKL, Moody GB, Peng CK, Mietus JE, Larson MG, Levy D, et al. Predicting survival in heart failure case and control subjects by use of fully automated methods for deriving nonlinear and conventional indices of heart rate dynamics. Circulation. 1997;96:842\u20138.","DOI":"10.1161\/01.CIR.96.3.842"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_017_w2aab3b7c18b1b6b1ab2ac17Aa","doi-asserted-by":"crossref","unstructured":"Goncalves H, Rocha AP, Ayres de Campos D, Bernardes J. Internal versus external intrapartum fetal heart rate monitoring: the effect on linear and nonlinear parameters. Physiol Meas. 2006;27:307.","DOI":"10.1088\/0967-3334\/27\/3\/008"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_018_w2aab3b7c18b1b6b1ab2ac18Aa","doi-asserted-by":"crossref","unstructured":"Ferrario M, Signorini MG, Magenes G. Complexity analysis of the fetal heart rate variability: early identification of severe intrauterine growth-restricted fetuses. Med Biol Eng Comput. 2009;47:911\u20139.","DOI":"10.1007\/s11517-009-0502-8"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_019_w2aab3b7c18b1b6b1ab2ac19Aa","doi-asserted-by":"crossref","unstructured":"Ferrario M, Signorini MG, Magenes G. Comparison between fetal heart rate standard parameters and complexity indexes for the identification of severe intrauterine growth restriction. Method Inform Med. 2007;46:186\u201390.","DOI":"10.1055\/s-0038-1625404"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_020_w2aab3b7c18b1b6b1ab2ac20Aa","doi-asserted-by":"crossref","unstructured":"Costa M, Goldberger AL, Peng C-K. Multiscale entropy analysis of biological signals. Phys Rev E. 2005;71:021906.","DOI":"10.1103\/PhysRevE.71.021906"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_021_w2aab3b7c18b1b6b1ab2ac21Aa","doi-asserted-by":"crossref","unstructured":"Costa M, Goldberger AL, Peng C-K. Multiscale entropy analysis of physiologic time series. Phys Rev Lett. 2002;89:062102.","DOI":"10.1103\/PhysRevLett.89.068102"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_022_w2aab3b7c18b1b6b1ab2ac22Aa","doi-asserted-by":"crossref","unstructured":"Goldberger AL, Amaral LAN, Glass L, Hausdorff JM, Ivanov PCh, Mark RG, et al. PhysioBank, PhysioToolkit, and PhysioNet: components of a new research resource for complex physiologic signals. Circulation. 2000;101:e215\u201320.","DOI":"10.1161\/01.CIR.101.23.e215"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_023_w2aab3b7c18b1b6b1ab2ac23Aa","doi-asserted-by":"crossref","unstructured":"Hjorth B, Elema-Sch\u00f6nander AB. EEG analysis based on time domain properties. Electroen Clin Neuro. 1970;2.2:306\u201310.","DOI":"10.1016\/0013-4694(70)90143-4"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_024_w2aab3b7c18b1b6b1ab2ac24Aa","doi-asserted-by":"crossref","unstructured":"Faul F, Erdfelder E, Buchner A, Lang A-G. Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Meth. 2009;41:1149\u201360.","DOI":"10.3758\/BRM.41.4.1149"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_025_w2aab3b7c18b1b6b1ab2ac25Aa","doi-asserted-by":"crossref","unstructured":"Fried PA, Watkinson B, Dillon RF, Dulberg CS. Neonatal neurological status in a low-risk population after prenatal exposure to cigarettes, marijuana, and alcohol. J Dev Behav Pediatr. 1987;8:318\u201326.","DOI":"10.1097\/00004703-198712000-00003"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_026_w2aab3b7c18b1b6b1ab2ac26Aa","unstructured":"Zeskind PS, Lester BM. The diagnostic utility of the assessment of infant cry sounds. In Zeskind PS, Singer L, editors. Biobehavioral assessment of the newborn and young infant. New York: Guilford Publications; 2001."},{"key":"2023040100110807885_j_jpm-2015-0275_ref_027_w2aab3b7c18b1b6b1ab2ac27Aa","doi-asserted-by":"crossref","unstructured":"Schuetze P, Zeskind, PS. Relation between maternal cigarette smoking during pregnancy and behavioral and physiological measures of autonomic regulation in neonates. Infancy. 2001;2:371\u201383.","DOI":"10.1207\/S15327078IN0203_5"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_028_w2aab3b7c18b1b6b1ab2ac28Aa","doi-asserted-by":"crossref","unstructured":"Oncken C, Kranzler H, O\u2019Malley P, Gendreau P, Campbell WA. The effect of cigarette smoking on fetal heart rate characteristics. Obstet Gynecol. 2002;99:751\u20135.","DOI":"10.1097\/00006250-200205000-00014"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_029_w2aab3b7c18b1b6b1ab2ac29Aa","doi-asserted-by":"crossref","unstructured":"Coppens M, Vindla S, James DK, Sahota DS. Computerized analysis of acute and chronic changes in fetal heart rate variation and fetal activity in association with maternal smoking. Am J Obstet Gynecol. 2001;185:421\u20136.","DOI":"10.1067\/mob.2001.115992"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_030_w2aab3b7c18b1b6b1ab2ac30Aa","doi-asserted-by":"crossref","unstructured":"Kapaya H, Pipkin FB, Hayes B, Loughna P. Smoking in pregnancy affects the fetal heart: possible links to future cardiovascular disease. J Matern Fetal Neonatal Med. 2014;15:1\u20135.","DOI":"10.3109\/14767058.2014.964202"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_031_w2aab3b7c18b1b6b1ab2ac31Aa","doi-asserted-by":"crossref","unstructured":"Graca LM, Cardoso CG, Clode N, Calhaz-Jorqe C. Acute effects of maternal cigarette smoking on fetal heart rate and fetal body movements felt by the mother. J Perinat Med. 1991;19:385\u201390.","DOI":"10.1515\/jpme.1991.19.5.385"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_032_w2aab3b7c18b1b6b1ab2ac32Aa","doi-asserted-by":"crossref","unstructured":"Zeskind P, Gingras J. Maternal cigarette-smoking during pregnancy disrupts rhythms in FHR. J Pediatr Psycol. 2005;31:5\u201314.","DOI":"10.1093\/jpepsy\/jsj031"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_033_w2aab3b7c18b1b6b1ab2ac33Aa","doi-asserted-by":"crossref","unstructured":"Renou P, Newman W, Wood C. Autonomic control of fetal heart rate. Am J Obstet Gynecol. 1969;105:949\u201353.","DOI":"10.1016\/0002-9378(69)90103-3"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_034_w2aab3b7c18b1b6b1ab2ac34Aa","doi-asserted-by":"crossref","unstructured":"Spyridou K, Chouvarda I, Hadjileontiadis L, Maglaveras N. CTG-based multipaarmetric risk stratification of pregnant women with smoking habit and pregnant women with IUGR. 6th European Conference of the International Federation for Medical and Biological Engineering OFMBE Proceedings. 2014;45:110\u20133.","DOI":"10.1007\/978-3-319-11128-5_28"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_035_w2aab3b7c18b1b6b1ab2ac35Aa","doi-asserted-by":"crossref","unstructured":"Rao RK, Yeragani VK. Decreased chaos and increased nonlinearity of heart rate time series in patients with panic disorder. Auton Neurosci. 2001;88:99\u2013108.","DOI":"10.1016\/S1566-0702(01)00219-3"},{"key":"2023040100110807885_j_jpm-2015-0275_ref_036_w2aab3b7c18b1b6b1ab2ac36Aa","doi-asserted-by":"crossref","unstructured":"Matthews T. Smoking during pregnancy in the 1990s. Natl Vital Stat Rep. 2001;49:1\u201314.","DOI":"10.1037\/e558942006-001"}],"container-title":["Journal of Perinatal Medicine"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.degruyter.com\/view\/j\/jpme.2017.45.issue-4\/jpm-2015-0275\/jpm-2015-0275.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.degruyter.com\/document\/doi\/10.1515\/jpm-2015-0275\/xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.degruyter.com\/document\/doi\/10.1515\/jpm-2015-0275\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,6,2]],"date-time":"2025-06-02T07:41:22Z","timestamp":1748850082000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.degruyter.com\/document\/doi\/10.1515\/jpm-2015-0275\/html"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,4,7]]},"references-count":36,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2016,7,30]]},"published-print":{"date-parts":[[2017,5,24]]}},"alternative-id":["10.1515\/jpm-2015-0275"],"URL":"https:\/\/doi.org\/10.1515\/jpm-2015-0275","relation":{},"ISSN":["1619-3997","0300-5577"],"issn-type":[{"value":"1619-3997","type":"electronic"},{"value":"0300-5577","type":"print"}],"subject":[],"published":{"date-parts":[[2016,4,7]]}}}