Abstract
This study aimed to assess the impact of obstructive sleep apnea (OSA) due to adenotonsillar hypertrophy (ATH) on the global myocardial performance in children using tissue Doppler imaging (TDI) and to evaluate the reversibility of the disorder after adenotonsillectomy (AT). The study included 42 children with OSA due to ATH (mean age, 5 ± 3.14 years) as the study group and 45 age- and sex-matched healthy children (mean age, 5.2 ± 3.08 years) as the control group. Polysomnography and echocardiography were performed. Indexed left ventricular mass (LVMi), pulmonary artery systolic pressure, mean pulmonary artery pressure (mPAP), and pulmonary vascular resistance (PVR) were calculated by echocardiography. Tissue Doppler imaging was used to determine the left ventricular and right ventricular myocardial performance index (MPI) of patients and control subjects before and after AT. The patients were classified into mild OSA (apnea-hypopnea index [AHI] 1–5; n = 18)] and moderate to severe OSA (AHI >5; n = 24) according to polysomnography findings. All the children in the control group had an AHI less than 1. They were treated using AT, then reevaluated by polysomnography and echocardiographic examination 6 to 8 months after surgery. Results are described as mean ± standard deviation. The patients with OSA had higher pulmonary artery systolic pressure, mPAP, PVR, LVMi, and right ventricular diastolic diameter than the control subjects. The patients with moderate to severe OSA showed more prominent changes than the patients with mild OSA, but the latter still differed significantly from the control subjects. The TDI-derived right ventricular MPI and left ventricular MPI measurements of the patients with OSA were higher (mean, 0.40 ± 0.08 vs 0.28 ± 0.01; p < 0.001) than those of the control subjects and (0.45 ± 0.05 vs 0.32 ± 0.05; p < 0.001) and correlated well with AHI and mPAP. In addition, mPAP was significantly correlated with AHI. Postoperatively, relief of OSA was validated by polysomnography, and a repeat of the echocardiographic parameters showed no significant differences between the patients and the control subjects. Tissue Doppler imaging can detect the subtle, subclinical changes in cardiac performance that occur in OSA due to adenotonsillar hypertrophy. Such changes generally are reversible after surgical treatment.
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References
AASM (2007) The AASM manual for the scoring of sleep and associated events rules, terminology, and technical specification. AASM, Westchester, IL, pp 48–49
Abbas AE, Fortuin FD, Schiller NB, Appleton CP, Moreno CA, Lester SJ (2003) A simple method for noninvasive estimation of pulmonary vascular resistance. J Am Coll Cardiol 41:1021–1027
Abd El-Moneim ES, Badawy BS, Atya M (2009) The effect of adenoidectomy on right ventricular performance in children. Int J Pediatr Otorhinolaryngol 73:1584–1588
Ali NJ, Pitson DJ, Stradling JR (1993) Snoring, sleep disturbance, and behavior in 4- to 5-year-olds. Arch Dis Child 68:360–366
American Academy of Sleep Medicine (2005) International classification of sleep disorders: diagnostic and coding manual, 2nd edn. American Academy of Sleep Medicine, Westchester, IL, pp 56–59
Amin RS, Kimball TR, Kalra M, Bean JA, Jeffries JL, Willging JP, Cotton RT, Witt SA, Glascock BJ, Daniels SR (2002) Left ventricular hypertrophy and abnormal ventricular geometry in children and adolescents with obstructive sleep apnea. Am J Respir Crit Care Med 165:1395–1399
Amin RS, Carroll JL, Jeffries JL, Grone C, Bean JA, Chini B, Bokulic R, Daniels SR (2004) Twenty-four-hour ambulatory blood pressure in children with sleep-disordered breathing. Am J Respir Crit Care Med 169:950–956
Amin RS, Kimball TR, Kalra M, Jeffries JL, Carroll JL, Bean JA, Witt SA, Glascock BJ, Daniels SR (2005) Left ventricular function in children with sleep-disordered breathing. Am J Cardiol 95:801–804
Bayram NA, Ciftci B, Bayram H, Keles T, Durmaz T, Akcay M, Yeter E, Bozkurt E (2008) Effects of continuous positive airway pressure therapy on right ventricular function assessment by tissue Doppler imaging in patients with obstructive sleep apnea syndrome. Echocardiography 25:1071–1078
Bayram NA, Ciftci B, Durmaz T, Keles T, Yeter E, Akcay M, Bozkurt E (2009) Effects of continuous positive airway pressure therapy on left ventricular function assessed by tissue Doppler imaging in patients with obstructive sleep apnoea syndrome. Eur J Echocardiogr 10:376–382
Brinker JA, Weiss JL, Lappé DL, Rabson JL, Summer WR, Permutt S, Weisfeldt ML (1980) Leftward septal displacement during right ventricular loading in man. Circulation 61:626–633
Brodsky L (1993) Tonsillitis, tonsillectomy, and adenoidectomy. In: Baily BJ (ed) Head and neck surgery-otolaryngology. JB Lippincott, Philadelphia, PA, pp 833–847
Brouillette RT, Thach BT (1979) A neuromuscular mechanism maintaining extrathoracic airway patency. J Appl Physiol 46:772–779
Brower CM, Gungor A (2000) Pediatric obstructive sleep apnea syndrome. Otolaryngol Clin North Am 33:49–75
Chan JY, Li AM, Au CT, Lo AF, Ng SK, Abdullah VJ, Ho C, Yu CM, Fok TF, Wing YK (2009) Cardiac remodelling and dysfunction in children with obstructive sleep apnoea: a community-based study. Thorax 64:233–239
Cloward TV, Walker JM, Farney RJ, Anderson JL (2003) Left ventricular hypertrophy is a common echocardiographic abnormality in severe obstructive sleep apnea and reverses with nasal continuous positive airway pressure. Chest 124:594–601
Cohn JN, Ferrari R, Sharpe N (2000) Cardiac remodeling: concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. International Forum on Cardiac Remodeling. Am Coll Cardiol 35:569–582
Corbo HM, Fuciarelli F, Foresi A, De Benedetto F (1989) Snoring in children: association with respiratory syndromes and passive smoking. BMJ 299:1491–1494 (published erratum appears in BMJ 1990;300:226)
Dabestani A, Mahan G, Gardin JM, Takenaka K, Burn C, Allfie A, Henry WL (1987) Evaluation of pulmonary artery pressure and resistance by pulsed Doppler echocardiography. Am J Cardiol 59:662–668
de Simone G, Daniels SR, Devereux RB, Meyer RA, Roman MJ, de Divitiis O, Alderman MH (1992) Left ventricular mass and body size in normotensive children and adults: assessment of allometric relations and impact of overweight. J Am Coll Cardiol 20:1251–1260
Devereux RB, Reichek N (1977) Echocardiographic determination of left ventricular mass in man: anatomic validation of the method. Circulation 55:613–618
Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N (1986) Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 57:450–458
Duman D, Naiboglu B, Esen HS, Toros SZ, Demirtunc R (2008) Impaired right ventricular function in adenotonsillar hypertrophy. Int J Cardiovasc Imaging 24:261–267
Ebeid MR, Ferrer PL, Robinson B, Weatherby N, Gebland H (1996) Doppler echocardiographic evaluation of pulmonary vascular resistance in children with congenital heart disease. J Am Soc Echocardiogr 9:822–831
Enright PL, Goodwin JL, Sherrill DL, Quan JR, Quan SF (2003) Blood pressure elevation associated with sleep-related breathing disorder in a community sample of white and Hispanic children. Tucson Children’s Assessment of Sleep Apnea Study. Arch Pediatr Adolesc Med 157:901–904
Friedberg MK, Feinstein JA, Rosenthal DN (2006) A novel echo-Doppler method for estimation of pulmonary arterial pressures. J Am Soc Echocardiogr 19:559–562
Galal O, Galal I (1989) Cor pulmonale as a sequela of tonsillar hypertrophy (in German). Monatsschr Kinderheilkd 137:326–329
Görür K, Döven O, Unal M, Akkuş N, Ozcan C (2001) Preoperative and postoperative cardiac and clinical findings of patients with adenotonsillar hypertrophy. Int J Pediatr Otorhinolaryngol 59:41–46
Greenfeld M, Tauman R, DeRowe A, Sivan Y (2003) Obstructive sleep apnea syndrome due to adenotonsillar hypertrophy in infants. Int J Pediatr Otorhinolaryngol 67:1055–1060
Guilleminault C, Eldridge FL, Simmons FB, Dement WC (1976) Sleep apnea in eight children. Pediatrics 59:23–30
Guilleminault C, Korobkin L, Winkle R (1981) A review of 50 children with obstructive sleep apnea. Lung 159:275–287
Harada K, Tamura M, Toyono M, Yasuoka K (1995) Effect of heart rate on left ventricular diastolic filling patterns assessed by Doppler echocardiography in normal infants. Am J Card 76:634–636
Harada K, Tamura M, Toyono M, Oyama K, Takada G (2001) Assessment of global left ventricular function by tissue Doppler imaging. Am J Cardiol 88:927–932, A9
Harada K, Tamura M, Toyono M, Yasuoka K (2002) Comparison of the right ventricular Tei index by tissue Doppler imaging to that obtained by pulsed Doppler in children without heart disease. Am J Cardiol 90:566–569
Hetzel M, Kochs M, Marx N, Woehrle H, Mobarak I, Hombach V, Hetzel J (2003) Pulmonary hemodynamics in obstructive sleep apnea: frequency and causes of pulmonary hypertension. Lung 181:157–166
Kawanishi Y, Ito T, Okuda N, Emura N, Hayashi T, Futai R, Yoneda H, Kitaura Y (2009) Alteration of myocardial characteristics and function in patients with obstructive sleep apnea. Int J Cardiol 133:129–131
Kepez A, Niksarlioglu EY, Hazirolan T, Ranci O, Kabul HK, Demir AU, Kaya EB, Kocabas U, Aytemir K, Sahin A, Tokgozoglu L, Nazli N (2009) Early myocardial functional alterations in patients with obstructive sleep apnea syndrome. Echocardiography 26:388–396
Kim SH, Cho GY, Shin C, Lim HE, Kim YH, Song WH, Shim WJ, Ahn JC (2008) Impact of obstructive sleep apnea on left ventricular diastolic function. Am J Cardiol 101:1663–1668
Kumar EB, Jaggarao NS (1989) Adenotonsillar hypertrophy and cor pulmonale: clinical and echocardiographic correlation. Postgrad Med J 65:473–475
Lai WW, Geva T, Shirali GS, Frommelt PC, Humes RA, Brook MM, Pignatelli RH, Rychik J (2006) Guidelines and standards for performance of a pediatric echocardiogram: a report from the Task Force of the Pediatric Council of the American Society of Echocardiography. J Am Soc Echocardiogr 19:1413–1430
Messner AH (1999) Evaluation of obstructive sleep apnea by polysomnography prior to pediatric adenotonsillectomy. Arch Otolaryngol Head Neck Surg 125:353–356
Miman MC, Kirazli T, Ozyurek R (2000) Doppler echocardiography in adenotonsillar hypertrophy. Int J Pediatr Otorhinolaryngol 54:21–26
Mitchell RB (2007) Adenotonsillectomy for obstructive sleep apnea in children: outcome evaluated by pre- and postoperative polysomnography. Laryngoscope 117:1844–1854
Nishimura RA, Abel MD, Hatle LK, Tajik AJ (1989) Assessment of diastolic function of the heart: background and current application of doppler echocardiography. Part 2. Clinical studies. Mayo Clin Proc 2:181–204
Okuda N, Ito T, Emura N, Suwa M, Hayashi T, Yoneda H, Kitaura Y (2007) Depressed myocardial contractile reserve in patients with obstructive sleep apnea assessed by tissue Doppler imaging with dobutamine stress echocardiography. Chest 131:1082–1089
Owen GO, Cater RJ, Robinson A (1996) Snoring, apnea, and ENT syndromes in the pediatric community. Clin Otolaryngol 21:130–134
Phillips B (2005) Sleep-disordered breathing and cardiovascular disease. Sleep Med Rev 9:131–140
Rojo EC, Rodrigo JL, Pérez de Isla L, Almería C, Gonzalo N, Aubele A, Cinza R, Zamorano J, Macaya C (2006) Disagreement between tissue Doppler imaging and conventional pulsed-wave Doppler in the measurement of myocardial performance index. Eur J Echocardiogr 7:356–364
Sahn DJ, DeMaria A, Kisslo J, Weyman A (1978) Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58:1072–1078
Sofer S, Weinhouse E, Tal A, Wanderman KL, Margulis G, Leiberman A, Gueron M (1988) Cor pulmonale due to adenoidal or tonsillar hypertrophy or both in children: noninvasive diagnosis and follow-up. Chest 93:119–122
Tavil Y, Kanbay A, Sen N, Ciftçi TU, Abaci A, Yalçin MR, Köktürk O, Cengel A (2007) Comparison of right ventricular functions by tissue Doppler imaging in patients with obstructive sleep apnea syndrome with or without hypertension. Int J Cardiovasc Imaging 23:469–477
Tei C, Ling LH, Hodge DO, Bailey KR, Oh JK, Rodeheffer RJ, Tajik AJ, Seward JB (1995) New index of combined systolic and diastolic myocardial performance: a simple and reproducible measurement of cardiac function: a study in normals and dilated cardiomyopathy. J Cardiol 26:357–366
Tei C, Dujardin KS, Hodge DO, Bailey KR, McGoon MD, Tajik AJ, Seward SB (1996) Doppler echocardiographic index for assessment of global right ventricular function. J Am Soc Echocardiogr 9:838–847
Tei C, Nishimura RA, Seward JB, Tajik AJ (1997) Noninvasive Doppler-derived myocardial performance index: correlation with simultaneous measurements of cardiac catheterization measurements. Am Soc Echocardiogr 10:169–178
Tugcu A, Guzel D, Yildirimturk O, Aytekin S (2009) Evaluation of right ventricular systolic and diastolic function in patients with newly diagnosed obstructive sleep apnea syndrome without hypertension. Cardiology 113:184–192
Tugcu A, Yildirimtürk O, Tayyareci Y, Demiroglu C, Aytekin S (2010) Evaluation of subclinical right ventricular dysfunction in obstructive sleep apnea patients using velocity vector imaging. Circ J 74:312–319
Ugur MB, Dogan SM, Sogut A, Uzun L, Cinar F, Altin R, Aydin M (2008) Effect of adenoidectomy and/or tonsillectomy on cardiac functions in children with obstructive sleep apnea. ORL J Otorhinolaryngol Relat Spec 70:202–208
Virolainen J, Ventilä M, Turto H, Kupari M (1995) Effect of negative intrathoracic pressure on left ventricular pressure dynamics and relaxation. J Appl Physiol 79:455–460
Waters KA, Cheng AT (2009) Adenotonsillectomy in the context of obstructive sleep apnoea. Paediatr Respir Rev 10:25–31
Weber SA, Montovani JC, Matsubara B, Fioretto JR (2007) Echocardiographic abnormalities in children with obstructive breathing disorders during sleep. J Pediatr (Rio J) 83:518–522
Wiatrak BJ, Wooly AL (1998) Pharyngitis and adenotonsillar disease. In: Fredrickson JM, Harker LA, Krause CJ, Richardson MA, Schuller DE, Cumings CW (eds) Otolaryngology, head and neck surgery. Mosby-Year Book Inc., Saint Louis, pp 188–215
Yasuoka K, Harada K, Toyono M, Tamura M, Yamamoto F (2004) Tei index determined by tissue Doppler imaging in patients with pulmonary regurgitation after repair of tetralogy of Fallot. Pediatr Cardiol 25:131–136
Yilmaz MD, Onrat E, Altuntaş A, Kaya D, Kahveci OK, Ozel O, Dereköy S, Celik A (2005) The effects of tonsillectomy and adenoidectomy on pulmonary arterial pressure in children. Am J Otolaryngol 26:18–21
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Attia, G., Ahmad, M.A., Saleh, A.B. et al. Impact of Obstructive Sleep Apnea on Global Myocardial Performance in Children Assessed by Tissue Doppler Imaging. Pediatr Cardiol 31, 1025–1036 (2010). https://doi.org/10.1007/s00246-010-9755-0
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DOI: https://doi.org/10.1007/s00246-010-9755-0