Abstract
A semi-automated processing approach was developed to assess the effects of early postnatal environmental tobacco smoke (ETS) on the cardiorespiratory control of newborn lambs. The system consists of several steps beginning with artifact rejection, followed by the selection of stationary segments, and ending with feature extraction. This approach was used in six lambs exposed to 20 cigarettes/day for the first 15 days of life, while another six control lambs were exposed to room air. On postnatal day 16, electrocardiograph and respiratory signals were obtained from a 6-h polysomnographic recording. The effects of postnatal ETS exposure on heart rate variability, respiratory rate variability, and cardiorespiratory interrelations were explored. The unique results suggest that early postnatal ETS exposure increases respiratory rate variability and decreases the coupling between cardiac and respiratory systems. Potentially harmful consequences in early life include unstable breathing and decreased adaptability of cardiorespiratory function, particularly during early life challenges, such as prematurity or viral infection.
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Alm B, Norvenius SG, Wennergren G, Skjærven R, Øyen N, Milerad J, Wennborg M, Kjaerbeck J, Helweg-Larsen K, Irgens LM (2001) Changes in the epidemiology of sudden infant death syndrome in Sweden 1973–1996. Arch Dis Child 84:24–30. https://doi.org/10.1136/adc.84.1.24
Bamford OS, Schuen JN, Carroll JL (1996) Effect of nicotine exposure on postnatal ventilatory responses to hypoxia and hypercapnia. Respir Physiol 106:1–11. https://doi.org/10.1016/0034-5687(96)00051-5
Berntson GG, Cacioppo JT, Quigley KS (1993) Respiratory sinus arrhythmia: autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology 30:183–196. https://doi.org/10.1111/j.1469-8986.1993.tb01731.x
Beuchée A, Nsegbe E, Hilaire MS, Carrault G, Branger B, Pladys P, Praud J-P (2007) Prolonged dynamic changes in autonomic heart rate modulation induced by acid laryngeal stimulation in non-sedated lambs. Neonatology 91:83–91. https://doi.org/10.1159/000097124
Beuchée A, Hernández AI, Duvareille C, Daniel D, Samson N, Pladys P, Praud J-P (2012) Influence of hypoxia and hypercapnia on sleep state-dependent heart rate variability behavior in newborn lambs. Sleep 35:1541–1549. https://doi.org/10.5665/sleep.2206
Blasi A, Jo J, Valladares E, Morgan BJ, Skatrud JB, Khoo MCK (2003) Cardiovascular variability after arousal from sleep: time-varying spectral analysis. J Appl Physiol 95:1394–1404. https://doi.org/10.1152/japplphysiol.01095.2002
Boardman A, Schlindwein FS, Rocha AP, Leite A (2002) A study on the optimum order of autoregressive models for heart rate variability. Physiol Meas 23:325–336. https://doi.org/10.1088/0967-3334/23/2/308
Borgnat P, Flandrin P, Honeine P, Richard C, Xiao J (2010) Testing stationarity with surrogates: a time-frequency approach. IEEE Trans Signal Process 58:3459–3470. https://doi.org/10.1109/TSP.2010.2043971
Carroll MS, Kenny AS, Patwari PP, Ramirez J-M, Weese-Mayer DE (2012) Respiratory and cardiovascular indicators of autonomic nervous system dysregulation in familial dysautonomia. Pediatr Pulmonol 47:682–691. https://doi.org/10.1002/ppul.21600
Cnaan A, Laird NM, Slasor P (1997) Using the general linear mixed model to analyse unbalanced repeated measures and longitudinal data. Stat Med 16:2349–2380. https://doi.org/10.1002/(SICI)1097-0258(19971030)16:20<2349::AID-SIM667>3.0.CO;2-E
Dahlström A, Ebersjö C, Lundell B (2008) Nicotine in breast milk influences heart rate variability in the infant. Acta Paediatr 97:1075–1079. https://doi.org/10.1111/j.1651-2227.2008.00785.x
Decarlo LT (1997) On the meaning and use of kurtosis. Psychol Meth 2:292–307. https://doi.org/10.1037/1082-989X.2.3.292
Dick TE, Hsieh Y-H, Dhingra RR, Baekey DM, Galán RF, Wehrwein E, Morris KF (2014) Cardiorespiratory coupling: common rhythms in cardiac, sympathetic, and respiratory activities. Prog Brain Res 209:191–205. https://doi.org/10.1016/B978-0-444-63274-6.00010-2
DiFranza JR, Aligne CA, Weitzman M (2004) Prenatal and postnatal environmental tobacco smoke exposure and children’s health. Pediatrics 113:1007–1015
Duvareille C, Beaudry B, St-Hilaire M, Boheimier M, Brunel C, Micheau P, Praud J-P (2010) Validation of a new automatic smoking machine to study the effects of cigarette smoke in newborn lambs. Lab Anim 44:290–297. https://doi.org/10.1258/la.2010.009124
Duvareille C, St-Hilaire M, Samson N, Bakirtzian P, Brisebois S, Boheimier M, Djeddi D-D, Doueik AA, Praud J-P (2013) Effects of postnatal environmental tobacco smoke on non-nutritive swallowing-breathing coordination in newborn lambs. Respir Physiol Neurobiol 185:446–453. https://doi.org/10.1016/j.resp.2012.08.014
Franco P, Chabanski S, Szliwowski H, Dramaix M, Kahn A (2000) Influence of maternal smoking on autonomic nervous system in healthy infants. Pediatr Res 47:215–220. https://doi.org/10.1203/00006450-200002000-00011
Galletly DC, Larsen PD (1997) Cardioventilatory coupling during anaesthesia. Br J Anaesth 79:35–40
Galletly DC, Larsen PD (1998) Relationship between cardioventilatory coupling and respiratory sinus arrhythmia. Br J Anaesth 80:164–168
GBD 2013 Mortality and Causes of Death Collaborators (2015) Global, regional, and national age–sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 385:117–171. https://doi.org/10.1016/S0140-6736(14)61682-2
Grönlund JU, Antila KJ, Siimes ASI, Metsälä T, Oja R, Tuominen J, Välimäki IAT (1989) Beta-adrenergic control and inter-relationships between heart rate and blood pressure in neonatal lambs. Med Biol Eng Comput 27:163–170. https://doi.org/10.1007/BF02446226
Grönlund JU, Kalli ST, Siimes AS, Sydänmaa M, Antila KJ, Välimäki IA (1991) Do beta-adrenergic blockade and sleep state affect cardiorespiratory control in neonatal lambs? Multivariate autoregressive modeling approach. Pediatr Res 29:272–277. https://doi.org/10.1203/00006450-199103000-00010
Hafström O, Milerad J, Sundell HW (2002) Prenatal nicotine exposure blunts the cardiorespiratory response to hypoxia in lambs. Am J Respir Crit Care Med 166:1544–1549. https://doi.org/10.1164/rccm.200204-289OC
Hafström O, Milerad J, Sundell HW (2004) Postnatal nicotine exposure does not further compromise hypoxia defense mechanisms in prenatally nicotine-exposed lambs. Acta Paediatr 93:545–551. https://doi.org/10.1080/08035250310023557
Hafström O, Milerad J, Sandberg KL, Sundell HW (2005) Cardiorespiratory effects of nicotine exposure during development. Respir Physiol Neurobiol 149:325–341. https://doi.org/10.1016/j.resp.2005.05.004
Harper RM (2000) Sudden infant death syndrome: a failure of compensatory cerebellar mechanisms? Pediatr Res 48:140–142. https://doi.org/10.1203/00006450-200008000-00004
Hassan M, Terrien J, Karlsson B, Marque C (2010) Interactions between uterine EMG at different sites investigated using wavelet analysis: comparison of pregnancy and labor contractions. EURASIP J Adv Signal Process 2010:918012. https://doi.org/10.1155/2010/918012
Hunt CE (1992) The cardiorespiratory control hypothesis for sudden infant death syndrome. Clin Perinatol 19:757–771
Hussein J, Farkas S, MacKinnon Y, Ariano RE, Sitar DS, Hasan SU (2007) Nicotine dose-concentration relationship and pregnancy outcomes in rat: biologic plausibility and implications for future research. Toxicol Appl Pharmacol 218:1–10. https://doi.org/10.1016/j.taap.2006.10.019
Javed F, Chan GSH, Middleton PM, Malouf P, Steel E, Savkin AV, Mackie J, Lovell NH (2009) Changes in the spectral powers of finger photoplethysmographic waveform variability in hemodialysis patients. In: 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Minneapolis, pp 3999-4002. https://doi.org/10.1109/IEMBS.2009.5333529
Kay SM (1998) Fundamentals of statistical signal processing. Volume II: detection theory. PTR Prentice-Hall signal processing series, Upper Saddle River
Larsen PD, Trent EL, Galletly DC (1999) Cardioventilatory coupling: effects of IPPV. Br J Anaesth 82:546–550
Li S, Lin J (2009) The optimal de-noising algorithm for ECG using stationary wavelet transform. In: 2009 WRI World Congress on Computer Science and Information Engineering, Los Angeles, pp 469–473. https://doi.org/10.1109/CSIE.2009.999
Liebrechts-Akkerman G, Lao O, Liu F, van Sleuwen BE, Engelberts AC, L’hoir MP, Tiemeier HW, Kayser M (2011) Postnatal parental smoking: an important risk factor for SIDS. Eur J Pediatr 170:1281–1291. https://doi.org/10.1007/s00431-011-1433-6
Loforte R, Carrault G, Mainardi L, Beuche A (2006) Heart rate and respiration relationships as a diagnostic tool for late onset sepsis in sick preterm infants. In: 2006 Computers in Cardiology, Valencia, pp 737–740
de Louw AV, Médigue C, Papelier Y, Cottin F (2008) Breathing cardiovascular variability and baroreflex in mechanically ventilated patients. Am J Phys 295:R1934–R1940. https://doi.org/10.1152/ajpregu.90475.2008
Mammone N, Morabito FC (2008) Enhanced automatic artifact detection based on independent component analysis and Renyi’s entropy. Neural Netw 21:1029–1040. https://doi.org/10.1016/j.neunet.2007.09.020
Manocha S, Girolami MA (2007) An empirical analysis of the probabilistic K-nearest neighbour classifier. Pattern Recogn Lett 28:1818–1824. https://doi.org/10.1016/j.patrec.2007.05.018
Mormann F, Lehnertz K, David P, Elger CE (2000) Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D: Nonlinear Phenomena 144:358–369. https://doi.org/10.1016/S0167-2789(00)00087-7
Motto AL, Galiana HL, Brown KA, Kearney RE (2004) Detection of movement artifacts in respiratory inductance plethysmography: performance analysis of a Neyman-Pearson energy-based detector. Conf Proc IEEE Eng Med Biol Soc 1:49–52. https://doi.org/10.1109/IEMBS.2004.1403087
Nakamura T, Horio H, Miyashita S, Chiba Y, Sato S (2005) Identification of development and autonomic nerve activity from heart rate variability in preterm infants. Biosystems 79:117–124. https://doi.org/10.1016/j.biosystems.2004.09.006
Navarro X, Porée F, Beuchée A, Carrault G (2015) Artifact rejection and cycle detection in immature breathing: application to the early detection of neonatal sepsis. Biomed Signal Process Control 16:9–16. https://doi.org/10.1016/j.bspc.2014.10.007
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC, Deepayan S, Team Rd, Sakar D, Bates CJ (2015) nlme: linear and nonlinear mixed effects models, version 3.1-120
Pinheiro J, Bates D, DebRoy S, Sarkar D, Eispack, Heisterkamp S, Van Willigen BV, R-core (2017) nlme: linear and nonlinear mixed effects models, version 3.1–131
Rajendra Acharya U, Paul Joseph K, Kannathal N, Lim CM, Suri JS (2006) Heart rate variability: a review. Med Biol Eng Comput 44:1031–1051. https://doi.org/10.1007/s11517-006-0119-0
Samson N, Dumont S, Specq M-L, Praud J-P (2011) Radio telemetry devices to monitor breathing in non-sedated animals. Respir Physiol Neurobiol 179:111–118. https://doi.org/10.1016/j.resp.2011.09.008
Savitzky A, Golay MJE (1964) Smoothing and differentiation of data by simplified least squares procedures. Anal Chem 36:1627–1639. https://doi.org/10.1021/ac60214a047
Schäfer C, Rosenblum MG, Abel HH, Kurths J (1999) Synchronization in the human cardiorespiratory system. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 60:857–870. https://doi.org/10.1103/PhysRevE.60.857
Schuetze P, Eiden RD (2006) The association between maternal smoking and secondhand exposure and autonomic functioning at 2–4 weeks of age. Infant Behav Dev 29:32–43. https://doi.org/10.1016/j.infbeh.2005.07.001
Schulz S, Bär K-J, Voss A (2015) Analyses of heart rate, respiration and cardiorespiratory coupling in patients with schizophrenia. Entropy 17:483–501. https://doi.org/10.3390/e17020483
Shi B, Zhang Y, Yuan C, Wang S, Li P (2017) Entropy analysis of short-term heartbeat interval time series during regular walking. Entropy 19:568. https://doi.org/10.3390/e19100568
Slotkin TA (2004) Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol Appl Pharmacol 198:132–151. https://doi.org/10.1016/j.taap.2003.06.001
Sobiech T, Buchner T, Krzesiński P, Gielerak G (2017) Cardiorespiratory coupling in young healthy subjects. Physiol Meas 38:2186–2202. https://doi.org/10.1088/1361-6579/aa9693
Somers VK, Dyken ME, Mark AL, Abboud FM (1993) Sympathetic-nerve activity during sleep in normal subjects. NEJM 328:303–307. https://doi.org/10.1056/NEJM199302043280502
St-Hilaire M, Samson N, Nsegbe E, Duvareille C, Moreau-Bussière F, Micheau P, Lebon J, Praud J-P (2007) Postnatal maturation of laryngeal chemoreflexes in the preterm lamb. J Appl Physiol 102:1429–1438. https://doi.org/10.1152/japplphysiol.00977.2006
Strasser F, Muma M, Zoubir AM (2012) Motion artifact removal in ECG signals using multi-resolution thresholding. In: 2012 Proceedings of the 20th European Signal Processing Conference (EUSIPCO), Bucharest, pp 899–903
Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93:1043–1065. https://doi.org/10.1161/01.CIR.93.5.1043
Trimer R, Cabidu R, Sampaio LLM, Stirbulov R, Poiares D, Guizilini S, Bianchi AM, Costa FSM, Mendes RG, Delfino A, Arena R, Borghi-Silva A (2014) Heart rate variability and cardiorespiratory coupling in obstructive sleep apnea: elderly compared with young. Sleep Med 15:1324–1331. https://doi.org/10.1016/j.sleep.2014.05.028
Tulppo MP, Mäkikallio TH, Takala TE, Seppänen T, Huikuri HV (1996) Quantitative beat-to-beat analysis of heart rate dynamics during exercise. Am J Phys 271:H244–H252. https://doi.org/10.1152/ajpheart.1996.271.1.H244
Vlemincx E, Abelson JL, Lehrer PM, Davenport PW, Van Diest I, Van den Bergh O (2013) Respiratory variability and sighing: a psychophysiological reset model. Biol Psychol 93:24–32. https://doi.org/10.1016/j.biopsycho.2012.12.001
von Borell E, Langbein J, Després G, Hansen S, Leterrier C, Marchant-Forde J, Marchant-Forde R, Minero M, Mohr E, Prunier A, Valance D, Veissier I (2007) Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals—a review. Physiol Behav 92:293–316. https://doi.org/10.1016/j.physbeh.2007.01.007
Zhang H, Zhu M, Zheng Y, Li G (2015) Toward capturing momentary changes of heart rate variability by a dynamic analysis method. PLoS One 10:e0133148. https://doi.org/10.1371/journal.pone.0133148
Acknowledgments
We would like to thank the biostatistician of the LTSI, Mrs. Nathalie Costet, for her assistance in the statistical analysis.
Funding
This study was supported by the Canada Research Chair in Neonatal Respiratory Physiology allocated to JP Praud and by the French Brittany council.
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All applicable guidelines from the Canadian Council on Animal Care were followed. All procedures performed in the present study involving animals were in accordance with the ethical standards of the University of Sherbrooke, where the studies were conducted.
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Al-Omar, S., Le Rolle, V., Beuchée, A. et al. Assessment of tobacco smoke effects on neonatal cardiorespiratory control using a semi-automated processing approach. Med Biol Eng Comput 56, 2025–2037 (2018). https://doi.org/10.1007/s11517-018-1827-y
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DOI: https://doi.org/10.1007/s11517-018-1827-y