Abstract
The association between obstructive sleep-disordered breathing (oSDB) and arterial stiffness, an independent predictor of cardiovascular outcomes, is not well established in children. This study compared cardiovascular parameters between healthy and oSDB children and aimed to identify predictors of arterial stiffness indices in children with oSDB. Cross-sectional study realized in a tertiary hospital from June 2018 to January 2020. Forty-eight children (3 to 10 years old) with clinical diagnosis of oSDB and indication for adenotonsillectomy and 24 controls were evaluated. Cardiovascular parameters were measured non-invasively by brachial artery oscillometry with a portable device. The main arterial stiffness indices assessed were augmentation index and pulse wave velocity, both derived from the aortic pulse wave. In the oSDB group, the questionnaires Obstructive Sleep Apnea-18 (OSA-18) and Pediatric Quality of Life Inventory version 4.0 (PedsQL 4.0) were applied. The oSDB group had higher values of reflection coefficient (p = 0.044) and augmentation index (p = 0.003) than the control group. Stepwise multiple regression analysis revealed that age, female sex, reflection coefficient, and systolic volume were independent predictors of augmentation index. Higher pulse wave velocity values were associated with worse quality of life assessed by PedsQL 4.0 questionnaire. There was no association with OSA-18. The vascular and hemodynamic parameters were similar in both groups.
Conclusion: Children with oSDB have increased augmentation index, an independent predictor of cardiovascular outcomes. The early identification of subclinical cardiovascular changes reinforces the importance of treating the disease, as well as changing lifestyle habits, to prevent complications in adulthood.
What is Known: • The association between oSDB and cardiovascular risk in adults is well described in the literature. • Children with oSDB, regardless of their weight or sex, have higher PWV values when compared to non-snoring children. | |
What is New: • Children with oSDB have augmented arterial stiffness, evidenced by the increase in AIx@75, measured non-invasively by brachial artery oscillometry with a portable device. • Low quality of life and therefore a high disease burden in children with oSDB may be a risk factor for arterial stiffness. |
Similar content being viewed by others
Data availability
All data is available in.pdf or.xls for appraisal.
Abbreviations
- AAO-HNS:
-
American Academy of Otolaryngology-Head and Neck Surgery
- AIx@75:
-
Augmentation index normalized to heart rate of 75 bpm
- AP:
-
Augmentation pressure
- BMI:
-
Body mass index
- cDBP:
-
Central diastolic blood pressure
- CI:
-
Cardiac index
- CO:
-
Cardiac output
- cPP:
-
Central pulse pressure
- cSBP:
-
Central systolic blood pressure
- HR:
-
Heart rate
- MAP:
-
Mean arterial pressure
- OSA-18:
-
Obstructive Sleep Apnea-18 questionnaire
- oSDB:
-
Obstructive sleep-disordered breathing
- pDBP:
-
Peripheral diastolic blood pressure
- PedsQL 4.0:
-
Pediatric Quality of Life Inventory, version 4.0
- PPA:
-
Pulse pressure amplification (pPP/cPP ratio)
- pPP:
-
Peripheral pulse pressure
- pSBP:
-
Peripheral systolic blood pressure
- PSG:
-
Polysomnography
- PWV:
-
Pulse wave velocity
- RC:
-
Reflection coefficient
- SV:
-
Systolic volume
- T&A:
-
Adenotonsillectomy
- TVR:
-
Total vascular resistance
References
Gipson K, Lu M, Kinane TB (2019) Sleep-disordered breathing in children. Pediatr Rev. https://doi.org/10.1542/pir.2018-0142
Kaditis AG, Alvarez MLA, Boudewyns A et al (2016) Obstructive sleep disordered breathing in 2- to 18-year-old children: diagnosis and management. Eur Respir J. https://doi.org/10.1183/13993003.00385-2015
Culebras A, Anwar S (2018) Sleep apnea is a risk factor for stroke and vascular dementia. Curr Neurol Neurosci Rep 18:53. https://doi.org/10.1007/s11910-018-0855-1
Cicero AFG, Morbini M, Urso R, Rosticci M, Parini A, Grandi E, D’Addato S, Borghi C (2016) Association between self-reported snoring and arterial stiffness: data from the Brisighella heart study. Intern Emerg Med 11:77–83. https://doi.org/10.1007/s11739-015-1310-9
Javaheri S, Barbe F, Campos-Rodriguez F et al (2017) Sleep apnea: types, mechanisms, and clinical cardiovascular consequences. J Am Coll Cardiol 69:841–858. https://doi.org/10.1016/j.jacc.2016.11.069
Vlahandonis A, Walter LM, Horne RSC (2013) Does treatment of SDB in children improve cardiovascular outcome? Sleep Med Rev 17:75–85. https://doi.org/10.1016/j.smrv.2012.04.004
Apostolidou MT, Alexopoulos EI, Damani E, Liakos N, Chaidas K, Boultadakis E, Apostolidis T, Gourgoulianis K, Kaditis AG (2008) Absence of blood pressure, metabolic, and inflammatory marker changes after adenotonsillectomy for sleep apnea in Greek children. Pediatr Pulmonol 43:550–560. https://doi.org/10.1002/ppul.20808
Ng DK, Wong JC, Chan CH, Leung LC, Leung SY (2010) Ambulatory blood pressure before and after adenotonsillectomy in children with obstructive sleep apnea. Sleep Med 11:721–725. https://doi.org/10.1016/j.sleep.2009.10.007
Horne RSC, Yang JSC, Walter LM et al (2011) Elevated blood pressure during sleep and wake in children with sleep-disordered breathing. Pediatrics 128:e85–e92. https://doi.org/10.1542/peds.2010-3431
Mitchell RB, Archer SM, Ishman SL et al (2019) Clinical practice guideline: tonsillectomy in children (update). Otolaryngol - Head Neck Surg (United States) 160:S1–S42. https://doi.org/10.1177/0194599818801757
Fernandes FMVS, Teles RDCVV (2013) Application of the Portuguese version of the obstructive sleep apnea-18 survey to children. Braz J Otorhinolaryngol 79:720–726. https://doi.org/10.5935/1808-8694.20130132
Lopes MT, Ferraro AA, Koch VHK, Lopes MT, Ferraro AA, Koch VHK (2015) Reliability of the Brazilian version of the PedsQL - ESDR questionnaire to evaluate quality of life of children and adolescents. J Bras Nefrol 37:158–165. https://doi.org/10.5935/0101-2800.20150026
Weber T, Wassertheurer S, Rammer M, Maurer E, Hametner B, Mayer CC, Kropf J, Eber B (2011) Validation of a brachial cuff-based method for estimating central systolic blood pressure. Hypertension 58:825–832. https://doi.org/10.1161/HYPERTENSIONAHA.111.176313
Flynn JT, Falkner BE (2017) New clinical practice guideline for the management of high blood pressure in children and adolescents. Hypertension 70:683–686. https://doi.org/10.1161/HYPERTENSIONAHA.117.10050
Shiraishi M, Murakami T, Higashi K (2020) The accuracy of central blood pressure obtained by oscillometric noninvasive method using Mobil-O-Graph in children and adolescents. J Hypertens 38:813–820. https://doi.org/10.1097/HJH.0000000000002360
Savant JD, Furth SL, Meyers KEC (2015) Arterial stiffness in children: pediatric measurement and considerations. Pulse 2:69–80. https://doi.org/10.1159/000374095
Torigoe T, Dallaire F, Slorach C, Cardinal MP, Hui W, Bradley TJ, Sarkola T, Mertens L, Jaeggi E (2020) New comprehensive reference values for arterial vascular parameters in children. J Am Soc Echocardiogr 33:1014-1022.e4. https://doi.org/10.1016/j.echo.2020.03.001
Walter LM, Tamanyan K, Limawan AP, Biggs SN, Weichard AJ, Davey MJ, Nixon GM, Horne RSC (2018) Overweight and obese children with sleep disordered breathing have elevated arterial stiffness. Sleep Med 48:187–193. https://doi.org/10.1016/j.sleep.2018.05.007
Montero López MP, Mora-Urda AI, Mill JG, Silva ABT, Santos Batista M, B Molina MDC (2019) Arterial stiffness and blood pressure in a multicultural child sample (Angola, Brazil, and Spain). Am J Hypertens 32:265–271. https://doi.org/10.1093/ajh/hpy182
Ayer JG, Harmer JA, Marks GB, Avolio A, Celermajer DS (2010) Central arterial pulse wave augmentation is greater in girls than boys, independent of height. J Hypertens 28:306–313. https://doi.org/10.1097/HJH.0b013e3283332286
Janner JH, Godtfredsen NS, Ladelund S, Vestbo J, Prescott E (2010) Aortic augmentation index: reference values in a large unselected population by means of the SphygmoCor device. Am J Hypertens 23:180–185. https://doi.org/10.1038/ajh.2009.234
Hidvégi EV, Illyés M, Molnár FT, Cziráki A (2015) Influence of body height on aortic systolic pressure augmentation and wave reflection in childhood. J Hum Hypertens 29:495–501. https://doi.org/10.1038/jhh.2014.118
Santos LM, Gomes IC, Pinho JF, Neves-Alves CM, Magalhaes GS, Campagnole-Santos MJ et al (2021) Predictors and reference equations for augmentation index, an arterial stiffness marker, in healthy children and adolescents. Clinics (Sao Paulo) 76. https://doi.org/10.6061/clinics/2021/e2350
McEniery CM, Yasmin HIR, Qasem A, Wilkinson IB, Cockcroft JR (2005) Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity - the Anglo-Cardiff collaborative trial (ACCT). J Am Coll Cardiol 46:1753–1760. https://doi.org/10.1016/j.jacc.2005.07.037
Protogerou AD, Safar ME (2007) Dissociation between central augmentation index and carotid-femoral pulse-wave velocity: when and why? Am J Hypertens 20:648–649. https://doi.org/10.1016/j.amjhyper.2007.02.008
Patil SP, Ayappa IA, Caples SM, John Kimoff R, Patel SR, Harrod CG (2019) Treatment of adult obstructive sleep apnea with positive airway pressure: an American academy of sleep medicine systematic review, meta-analysis, and GRADE assessment. J Clin Sleep Med 15:301–334. https://doi.org/10.5664/jcsm.7638
Arnardottir ES, Maislin G, Jackson N, Schwab RJ, Benediktsdottir B, Teff K, Juliusson S, Pack AI, Gislason T (2013) The role of obesity, different fat compartments and sleep apnea severity in circulating leptin levels: the Icelandic Sleep Apnea Cohort study. Int J Obes (Lond) 37:835–842. https://doi.org/10.1038/ijo.2012.138
Tap L, Dommershuijsen LJ, Corsonello A, Lattanzio F, Bustacchini S, Ziere G, van Saase JLCM, Mattace-Raso FUS (2020) The possible impact of aortic stiffness on quality of late life: an exploratory study. Clin Interv Aging 15:133–140. https://doi.org/10.2147/CIA.S239186
Al Mheid I, Veledar E, Martin GS, Vaccarino V, Quyyumi AA (2014) Functional health and well-being, arterial stiffness and vascular dysfunction in healthy adults. Int J Cardiol 174:729–730. https://doi.org/10.1016/j.ijcard.2014.04
García-Ortiz L, Recio-Rodríguez JI, Mora-Simón S et al (2016) Vascular structure and function and their relationship with health-related quality of life in the MARK study. BMC Cardiovasc Disord. https://doi.org/10.1186/s12872-016-0272-9
Vlachopoulos C, Aznaouridis K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol 55:1318–1327. https://doi.org/10.1016/j.jacc.2009.10.061
Li WF, Huang YQ, Feng YQ (2019) Association between central haemodynamics and risk of all-cause mortality and cardiovascular disease: a systematic review and meta-analysis. J Hum Hypertens 33:531–541. https://doi.org/10.1038/s41371-019-0187-x
Duarte SV, de Souza Rajão R, Pinho JF, Dos Santos LM, Alves-Neves CM, Magalhães GS, Ribeiro-Oliveira A, Rodrigues-Machado MDG (2019) Changes in aortic pulse wave components, pulse pressure amplification, and hemodynamic parameters of children and adolescents with type 1 diabetes. Pediatr Diabetes 20:202–209. https://doi.org/10.1111/pedi.12782
Bhattacharjee R, Kheirandish-Gozal L, Spruyt K et al (2010) Adenotonsillectomy outcomes in treatment of obstructive sleep apnea in children: a multicenter retrospective study. Am J Respir Crit Care Med 182:676–683. https://doi.org/10.1164/rccm.200912-1930OC
Huang YS, Guilleminault C, Lee LA, Lin CH, Hwang FM (2014) Treatment outcomes of adenotonsillectomy for children with obstructive sleep apnea: a prospective longitudinal study. Sleep 37:71–76. https://doi.org/10.5665/sleep.3310
Author information
Authors and Affiliations
Contributions
Rossi-Monteiro, EM: selected the patients; conceived and outlined the study; coordinated and supervised the data collection; analyzed and interpreted the data; drafted, edited, and critically reviewed the manuscript for important intellectual content. Sefair, LR; Lima, MC; Nascimento, MFL: contributed to the data collection and reviewed the manuscript for important intellectual content. Rodrigues-Machado, MG: conceived and designed the study; analyzed and interpreted the data; drafted, edited, and critically revised the manuscript for important intellectual content. Mendes-Pinto, D; Anschuetz, L: revised the manuscript for important intellectual content. All the authors read and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the Bioethics Committee of the Faculdade Ciências Médicas de Minas Gerais under the protocol number 08812019000005134.
Consent to participate
Informed assent was obtained from all minors’ participants included in the study. Written informed consent was obtained from the parents or legal guardians.
Consent for publication
All parents or legal guardians have signed informed consent regarding publishing data about their children.
Competing interests
The authors declare no competing interests.
Additional information
Communicated by Peter de Winter
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rossi-Monteiro, E.M., Sefair, L.R., Lima, M.C. et al. Pediatric obstructive sleep-disordered breathing is associated with arterial stiffness. Eur J Pediatr 181, 725–734 (2022). https://doi.org/10.1007/s00431-021-04238-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00431-021-04238-1