- Email: [email protected]
The effects of adenotonsillar hypertrophy corrective surgery on left ventricular functions and pulmonary artery pressure in children
International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: http://www.ijporlonline.com/
The effects of adenotonsillar hypertrophy corrective surgery on left ventricular functions and pulmonary artery pressure in children Mecnun Çetin a, *, Nazım Bozan b a b
Department of Pediatric Cardiology, Yuzuncu Yil University, Van, Turkey Department of Otolaryngology, Yuzuncu Yil University, Van, Turkey
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 July 2017 Accepted 20 July 2017 Available online 22 July 2017
Objective: Comparison of left ventricular functions in preoperative and postoperative periods of children with adenotonsillar hypertrophy (ATH) who have findings of upper airway obstruction (UAO), using echocardiographic parameters. Methods: Thirty children who were diagnosed with UAO due to ATH, and who have undergone adenoidectomy/adenotonsillectomy and 30 healthy children, between 2 and 11 years of age, were included in the study. Patient group was evaluated by the pulsed wave tissue Doppler echocardiography, as well as with conventional echocardiography, before and 6 months after the operation. Results: Of 30 children in study group, 18 (60%) had adenotonsillectomy and 12 (40%) had adenoidectomy. The differences between groups regarding myocardial performance index (MPI) was not statistically significant (p ¼ 0.847). There was not any statistically significant difference between groups in terms of mitral isovolemic acceleration (MIVA) (2.28 ± 0.67, 2.24 ± 0.55, 2.23 ± 0.49; p ¼ 0.943, respectively). Interventricular septum diameter (IVSD) was significantly higher in preoperative group than postoperative and control groups (3.68 ± 0.52, 3.50 ± 0.40, 3.38 ± 0.60; p ¼ 0.028, respectively). Pulmonary acceleration time (PAcT) was found to be significantly lower in preoperative group compared to postoperative and control groups (107.64 ± 16.60, 119.52 ± 15.95, 120.47 ± 16.19; p ¼ 0.004, respectively). Mean pulmonary arterial pressure (mPAP) was significantly higher in preoperative group than postoperative and control groups (30.58 ± 8.11, 25.23 ± 9.07, 25.00 ± 6.52; p ¼ 0.002, respectively). In postoperative group mPAP was found to be similar to the control group. Conclusions: Clinical or subclinical left ventricle (LV) dysfunction in children with ATH who have findings of UAO was not determined while mean pulmonary arterial pressure was significantly higher compared with the control cases. Besides early adenotonsillectomy is a beneficial treatment option for these patients. © 2017 Elsevier B.V. All rights reserved.
Keywords: Adenotonsillar hypertrophy (ATH) Left ventricle (LV) Tissue doppler echocardiography
1. Introduction Upper airway obstruction (UAO) during sleep comprises a large spectrum of symptoms varying from night time snoring to the obstructive sleep apnea-hypopnea syndrome. The most common symptoms defined are the snoring, respiratory pauses, difficulty in breathing, agitated sleep and nocturnal diaphoresis [1]. Adenotonsillar hypertrophy (ATH), the excessive lymphoid tissue proliferation on adenoids and tonsils, is the most common cause of upper air-way obstruction in pediatric population [2e4].
* Corresponding author. Tel.: þ90 432 215 0473; fax: þ90 432 216 83 52. E-mail address: [email protected] (M. Çetin). http://dx.doi.org/10.1016/j.ijporl.2017.07.027 0165-5876/© 2017 Elsevier B.V. All rights reserved.
Severe UAO can result in chronic alveolar hypoventilation, which may cause hypoxemic pulmonary vasoconstriction and the resulting rise in pulmonary vascular resistance and pulmonary arterial pressure (PAP). Dilatation and hypertrophy of the right side of the heart and subsequent right ventricular dysfunction are the end results of persistent pulmonary vascular resistance [5,6]. Early recognition of ventricular dysfunction is important in prevention of further progression to heart failure and even death and also in decision of requirement of surgical treatment [7,8]. Recently, tissue Doppler echocardiography (TDI) has been defined as a reliable and accurate technique in evaluation of global and regional ventricular functions [9]. Although the data in literature is conflicting, majority of studies suggest that severe UAO contributes to the development of left
42
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
ventricular systolic and diastolic dysfunctions and subsequently heart failure [10]. However, the exact pathophysiological mechanisms linking UAO to cardiovascular disease or the long-term impacts of UOA on cardiovascular system were not defined clearly, yet. Even though there are many studies about the effects of ATH on left ventricle functions in adults [11,12], and there are many studies in children dealing with the effects of ATH on right ventricle; the data about the association of ATH with left ventricle functions in children is limited. The objective of this study was to evaluate the left ventricle (LV) functions in children with ATH, by means of TDI, and to determine the effects of adenotonsillectomy on LV functions by comparing pre- and post-operative data. 2. Methods The study protocol was approved by the University of Yuzuncu Yil Ethics Committee. Informed consent was obtained from parents of the participants. Thirty patients (17 male, 13 female, mean age 5.8 ± 3.0 years) with history and physical examination findings suggestive of UAO, who have undergone adenoidectomy/adenotonsillectomy due to stage III or stage IV adenoid and/or ATH were included in the study. In control group, there were 30 healthy children (15 male, 15 female, mean age 5.9 ± 2.1 years) who were admitted to pediatric cardiology outpatient clinic with murmur, syncope, or chest pain and whose echocardiographic evaluations revealed no pathologic findings. The participants were selected consecutively. A questionnaire was applied to the study group with the purpose of determining whether there were symptoms related to upper respiratory tract obstruction (snoring, respiratory arrest during sleep, open mouth, sleeping, suddenly waking up at night, nocturnal diuresis, mouth open navigation and sleepiness during the day) (Table 3). Parents were asked to answer the questions in questionnaire. Answers such as always, frequently and yes were considered as positive and the ones like sometimes, never, and no were considered as negative responses. Exclusion criteria were as follows: presence of additional pathologies leading to UAO other than ATH, heart disease with congenital origin or secondary to another disease, primary pulmonary hypertension, any systemic diseases, obesity, craniofacial anomaly, and genetic syndrome or inability to obtain informed consent from family. Detailed histories of the patients were obtained and comprehensive physical examination including height, weight, and arterial blood pressure measurements were performed in all participants. Degree of tonsillar hypertrophy of the study group was determined with paranasal sinus radiographs and clinical findings, according to the Brodsky scale, regarding the degree of oropharyngeal obstruction due to palatine tonsils [13]. Examination of adenoids was performed by fibreoptic endoscopy. According to this evaluation, percentage of obstruction of the passage by adenoids was determined and staging was performed [14]. Conventional Doppler echocardiography (CDE) and TDI values for all patients were recorded. Study group was evaluated by echocardiography in preoperative period and on 6th month after operation.
2.2. Echocardiography Echocardiography was performed on the left lateral decubitus and supine positions with an ultrasound machine Vivid 6S (GEVingmed Ultrasound AS, Horten, Norway) and 3S-RS (3.5 Mhz) probe. Averages of three consecutive cycles were measured for all echocardiographic data. Images were obtained from parasternal and apical positions using 2D, M-mode and Doppler echocardiographic techniques. M-mode echocardiographic measurements were performed according to standards outlined by the American Society of Echocardiography [15]. The following variables were measured: interventricular septum diameter (IVSD), left ventricle fractional shorting (LVFS), left ventricle (LV) diameter and LV posterior wall thickness (LVpWD). IVSD and LVpWD were measured at the end of diastole in parasternal long axis. Left ventricular end-diastolic (LVedD) and end-systolic diameter (LVesD) were measured at the end of systole and diastole in parasternal long axis. LVFS was calculated as the percentage decrease of LV systolic diameter to the diastolic diameter. The pulmonary acceleration time (PAcT), pulmonary peak velocity (PPV) and pulmonary ejection time (PET) were obtained using the pulse wave Doppler with the pulse wave sample volume placed within the RV outflow tract. PET was measured as the time from onset to completion of systolic pulmonary flow. PAcT is the time interval between the onset of the systolic velocity and the peak systolic velocity [16]. Using this measurement, the mean pulmonary artery pressure (mPAP) was calculated by the equation (Mahan formula): mPAP ¼ 79e (0.45 PAcT) [17,18]. TDI was recorded from the apical 4C view with the pulse wave Doppler sample volume placed on the mitral lateral annulus. Peak systolic (Sm) velocity, peak early (Em), the deceleration time (DT) of Em wave and peak late (Am) diastolic myocardial annular velocity, isovolemic relaxation time (IVRT), and isovolemic contraction time (IVCT) were measured. Myocardial performance index (MPI) was calculated with the Tei index formula. Mitral isovolemic acceleration (MIVA) for the LV was calculated by dividing the isovolemic contraction peak velocity by the time interval between the onset of this wave and its peak velocity [19,20] (Fig. 1). Examinations were performed by single experienced pediatric cardiologists.
2.1. Operative management Preoperative routine anesthetic evaluations were including blood tests and chest X-ray. All children were operated as inpatient and under general anesthesia. Adenoidectomy in 12 patients and adenotonsillectomy in 18 patients were carried out by curettage and cold dissection methods. Postoperative period care was uneventful in all children. The average period of hospital stay was two days.
Fig. 1. Calculation of left ventricular MPI and MIVA with TDI. MIVA, mitral isovolumic acceleration; IVV, isovolumic contraction peak velocity; AcT, acceleration time; Sm, systolic myocardial velocity; Em, early diastolic myocardial velocity; Am, late diastolic myocardial velocity; IVRT, isovolumic relaxation time; IVCT, isovolumic contraction time; ET, ejection time; MPI, myocardial performance index.
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
43
Table 1 General characteristics of the study population (mean ± SD). SBP, systolic blood pressure; DBP, diastolic blood pressure.
Age (years) Sex (male/female) Weight (kg) Height (cm) SBP (mmHg) DBP (mmHg) Heart rate (beats/min)
Preop (n ¼ 30)
Postop (n ¼ 30)
Control (n ¼ 30)
P
5.8 þ 3.0 17/13 22.4 þ 7.1 114 þ 13 93.0 þ 7.2 57.7 þ 7.1 96.2 þ 9.5
5.8 þ 3.0 17/13 22.4 þ 7.1 114 þ 13 96.1 þ 10.0 59.4 þ 9.0 93.8 þ 13.1
5.9 þ 2.1 15/15 23.5 þ 5.9 115 þ 10 91.4 þ 8.8 55.4 þ 9.4 95.4 þ 10.2
0.853 0.545 0.723 0.907 0.110 0.213 0.691
2.3. Statistical analysis Statistical analyses were performed with the SPSS (ver: 15.0) statistical program. Descriptive statistics for the continuous variables were presented as mean ± standard deviation; minimum and maximum values while count and percentages for categorical variables. One-way ANOVA was used to compare the group means. Duncan multiple comparison test was also used to identify different group means followed by ANOVA. In addition, chi-square test was performed to determine the relationship between categorical variables. Statistical significance level was considered as 0.05. 3. Results Seventeen of 30 patients in the study group (56.6%) and 15 of the 30 patients in the control group (50%) were male. Age, gender, weight, height, blood pressure and heart rate were not statistically significantly different between 2 groups (Table 1). Twelve patients (40%) in study group had adenoidectomy while 18 (60%) were operated for adenotonsillectomy (Table 2). When the symptoms of patients were investigated; during preoperative period all 30 patients in the study group were having snoring symptoms. Snoring complaint which was present in all of 30 patients disappeared in 23 of them, postoperatively. Of 22 patients with ATH, 20 reported that their complaints improved. As a result, all complaints of the patients revealed statistically significant differences between preoperative and postoperative periods (Table 3). 3.1. Echocardiographic data In the assessment made by M-mode echocardiography, IVSD
Table 2 The degree of adenoid and tonsillar hypertrophy of the study group. Type of operation
Grade II n (%)
Grade III n (%)
Grade IV n (%)
Total n (%)
Tonsillectomy Adenoidectomy
3 (16.6) 0 (0)
12 (66.8) 20 (66.7)
3 (16.6) 10 (33.3)
18 (100) 30 (100)
was significantly higher in preoperative group than postoperative and control groups (3.68 ± 0.52, 3.50 ± 0.40, 3.38 ± 0.60; p ¼ 0.028, respectively). The difference between postoperative and control groups was not significant (p > 0.05). There was not any statistically significant difference between the groups, in terms of LVpWD, LVesD, LVedD and LVFS (Table 4). PAcT obtained by CDE was significantly lower in preoperative group (p ¼ 0.004). Also mPAP was significantly higher in preoperative group compared to other 2 groups (p ¼ 0.002) (Fig. 2). Any significant difference was not detected between postoperative and control groups regarding all variables (Table 4). In evaluation of LV TDI; There was not any statistically significant difference between the groups, in terms of MIVA (2.28 ± 0.67, 2.24 ± 0.55, 2.23 ± 0.49; p ¼ 0.943, respectively). The differences in MPI values in preoperative, postoperative and control groups were not statistically significant (0.38 ± 0.07, 0.35 ± 0.06, 0.36 ± 0.06; p ¼ 0.847, respectively). There was also not any significant difference between groups, in terms of other variables (p > 0.05) (Table 5). 4. Discussion The data about the LV functions in children with ATH is limited. In this study we evaluated the effects of ATH in children who have findings of UAO on pulmonary system and LV functions by CDE and TDI and we have determined that after adenotonsillectomy the symptoms of patients significantly improved. Regarding the echocardiographic data, we did not determine a significant difference between groups in terms of LV functions including LVpWD, LVedD, LVesD or LVFS; however IVSD was significantly higher together with the mPAP in preoperative group. The most common cause of UAO in children is the ATH. The development of pulmonary hypertension and heart dysfunction in patients with chronic UAO is complex. Respiratory acidosis induced by hypoxemia and hypercarbia is the main mediator of pulmonary vasoconstriction that can lead to reversible or irreversible chronic changes in the pulmonary vasculature. Moreover, various neurohumoral factors produced in response to respiratory distress may additionally promote pulmonary hypertension, right ventricular dysfunction, and consequent impairment of systemic cardiac output [2,21,22].
Table 3 The patient's preoperative and postoperative symptoms. Preoperative
Snoring Stop breathing during sleep Open mouth breathing Suddenly waking up at night Enuresis Open mouth during daytime Daytime sleepiness
Postoperative
P
Yes n (%)
No n (%)
Yes n (%)
No n (%)
30 (100) 22 (73.4) 28 (93.4) 12 (40) 4 (13.3) 17 (56.6) 5 (16.6)
0 (0) 8 (26.6) 2 (6.6) 18 (60) 26 (86.7) 13 (43.4) 25 (83.4)
7 2 6 0 1 3 0
23 28 24 30 29 27 30
(23.3) (6.6) (20) (0) (3.3) (10) (0)
(76.7) (93.4) (80) (100) (96.7) (90) (100)
<0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05
44
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
Table 4 Left ventricular 2D echocardiographic measurements of groups, and pulmonary flow evaluations and mPAP values obtained by conventional dopppler echocardiography (mean ± SD). LVpWD, left ventricle posterior wall diameter; LVedD, left ventricle end-diastolik diameter; LVesD, left ventricle end-sistolik diameter; LVFS, fractional shorting of left ventricle; IVSD, interventriculare septum diamater. PET, pulmonary ejection time; PPV, pulmoner peak velocity; PAcT, acceleration time; mPAP, mean pulmonary artery pressure.
LVpWD (mm) LVedD (mm) LVesD (mm) LVFS IVSD (mm) PET (msn) PAcT (msn) PPV (m/sn) mPAP (mmHg)
Preop (n ¼ 30)
Postop (n ¼ 30)
Control (n ¼ 30)
P
3.66 ± 0.4 34.6 ± 2.9 24.3 ± 3.8 30.77 ± 3.5 3.68 ± 0.52a 267.9 ± 21.2 107.6 ± 16.6b 0.98 ± 0.13 30.58 ± 8.11a
3.81 ± 0.4 34.7 ± 3.6 23.4 ± 3.4 32.56 ± 5.2 3.50 ± 0.40a 278.2 ± 19.6 119.5 ± 15.9b 1.05 ± 0.09 25.23 ± 9.07b
3.71 ± 0.7 35.2 ± 3.9 23.3 ± 3.5 34.09 ± 2.9 3.38 ± 0.60b 269.9 ± 12.4 120.4 ± 16.1a 1.01 ± 0.13 25.00 ± 6.52b
0.584 0.772 0.519 0.123 0.028 0.076 0.004 0.130 0.002
Table 5 LV TDI values of groups (mean ± SD). Sm, systolic myocardial velocity; Em, early diastolic myocardial velocity; Am, late diastolic myocardial velocity; DT, deceleration time; IVRT, isovolumic relaxation time; IVCT, isovolumic contraction time; ET, ejection time; MPI, myocardial performance index; MIVA, mitral isovolumic acceleration.
Sm (cm/sn) Em (cm/sn) Am (cm/sn) Em/Am DT (msn) IVRT (msn) IVCT (msn) ET (msn) MPI MIVA (m/sn2)
Preop (n ¼ 30)
Postop (n ¼ 30)
Control (n ¼ 30)
P
8.91 ± 2.80 17.55 ± 3.08 6.75 ± 1.89 2.60 ± 0.85 75.42 ± 13.27 42.45 ± 11.34 58.64 ± 16.46 265.6 ± 20.2 0.38 ± 0.07 2.28 ± 0.67
9.44 ± 0.41 17.06 ± 2.56 6.46 ± 1.65 2.98 ± 0.68 76.11 ± 11.74 42.09 ± 9.60 53.45 ± 8.47 274.5 ± 22.1 0.35 ± 0.06 2.24 ± 0.55
8.93 ± 1.32 18.42 ± 2.81 6.42 ± 1.53 2.71 ± 0.63 74.09 ± 13.66 43.38 ± 9.16 52.09 ± 11.68 268.2 ± 15.0 0.36 ± 0.06 2.23 ± 0.49
0.791 0.174 0.726 0.127 0.580 0.877 0.340 0.196 0.847 0.943
a,b
; The different lower cases represent statistically significant difference.
Until the rapid onset of severe cardiac decompensation occurs, progressive pulmonary hypertension may cause minimal symptoms. In that aspect, for the decision of early surgical approach detection of subclinical cardiac impairment is crucial. Eventually, a reliable, noninvasive, and simple method is desirable for the decision of early surgical treatment. Elevated PAP values associated with ATH in children were reported before those were mostly reversible after adenotonsillectomy [23e25]. Jabbari et al. evaluated the changes of preadentonsillectomy echocardiographic findings after adenotonsillectomy and reported that severe chronic ATH caused higher tricuspid regurgitation pressure and mean pulmonary arterial pressure that were improved after adenotonsillectomy [26]. Recently, Orji et al. reported a significant decrease in mPAP values after adenotonsillectomy in 39 children with ATH. They also reported that, in 14 of 17 children with pulmonary hypertension, mPAP decreased to normal range 6 weeks after operation [27]. In our study, in preoperative group PAcT value, which is inversely correlated with mPAP, was found to be significantly lower compared to postoperative and control group. The PAcT values at 6 month after operation and control group was found to be similar. In the same way, mPAP was significantly higher in preoperative group. In postoperative group mPAP was similar to control group.
Children with obstructive respiratory disorders during sleep are exposed to repeated hypopnea and apnea periods. Hypercapnia and hypoxemia that take place during apnea periods provoke respiratory acidosis and resulting vasoconstriction of the pulmonary artery. Throughout sleeping, decubitus horizontal position and intra-thoracic pressure which becomes more negative due to respiratory effort against the obstruction also increase venous return to the right-hand cardiac chambers, in addition to increased pulmonary resistance. Right ventricle volume increases with an increase in venous return that alters the position of interventricular septum through left ventricle which in turn decreases the left ventricle compliance and end-disatolic volume. The augmented negativity of intra-thoracic pressure also alters the balance between extra- and intra-cardiac pressures and increases the transmural pressure of left ventricle. With the effects of negative intrathoracic pressure, the blood flow through thoracic aorta becomes more difficult increasing the left ventricle afterload. Those alterations can lead to ventricular global dysfunction [1,28e30]. There are some studies in literature evaluating left ventricle functions in children with ATH or OSAS. Amin et al. reported an abnormal LV geometry in 15% of 19 children with habitual snoring and in 39% of 28 children with OSAS, and OSAS was associated with €rür et al. on increased LV mass in children [31]. In a study of Go children with ATH, LVedD and IVSD values were reported to be significantly higher in preoperative group [32]. In another study in
Fig. 2. Distribution of mPAP between groups, Statistically significant difference was determined between groups, p < 0.05.
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
children with moderate-severe OSAS, left ventricular ejection fraction and LVFS were determined to be lower compared with patients having mild OSAS or primary snoring and the authors defined a negative correlation between LV systolic functions and the degree of UAO [33]. In our study we did not determine a significant difference between groups regarding LVpWD, LVedD, LVesD or LVFS. However, IVSD showed a significant increase in preoperative group compared with control group and although there was a gradual decrease in IVSD in postoperative group compared with the preoperative values. We believe that, this increase in IVSD was due to the RV hypertrophy secondary to the increased pressure in pulmonary system. In a study of Attia et al. on children with OSAS, preoperative MPI value was defined to be significantly decreased in postoperative period and in patients with OSAS secondary to ATH, subclinical alterations in LV were determined with DDI [34]. In another study on children with ATH, DT determined on mitral valve was elongated in patient group compared with the control group which also normalized after adenotonsillectomy and the cause of this elongation was defined as diastolic dysfunction in LV [32]. Cincin et al. reported that, both the LV and RV MPI significantly improved after surgery for ATH [35]. In our study, contrary with the literature, there was not any statistically significant difference between groups regarding systolic and diastolic LV measurements obtained by DDE. Although IVCT and MPI were longer in preoperative group, the differences were not statistically significant. With those findings, at least at that level, we did not determine left ventricular systolic or diastolic dysfunction in study group. The IVA evaluates myocardial motion during the isovolumetric contraction period and it has been validated as a sensitive noninvasive index of LV and RV. The rate of myocardial acceleration during the isovolemic period has been described to correlate with intrinsic myocardial contractility and is thought to be relatively independent of loading conditions [36]. We did not determine any alterations regarding MIVA in patients with ATH in this study. The main limitation of this study is the lack of polysomnographic evaluations. However, it is not feasible to perform polysomnographic evaluations in children and moreover this study is not evaluating the patients with ATH or obstructive sleep apnea; instead we have investigated the patients with the symptoms of upper airway obstruction. In our study, among patients with ATH that were considered to have UAO, significant benefits of adenotonsillectomy were observed based on symptoms. Moreover, with conventional echocardiography, we determined that in patients with ATH pulmonary arterial pressure was higher in preoperative period and improved to normal values with adenotonsillectomy. However, in this study evaluating LV with TDI, contrary with the literature, we did not determine any findings of clinical or subclinical left ventricular dysfunction. In the light of these data, we believe that left ventricular dysfunction does not develop in a short time period in childhood as suggested before. The increased MPI values determined in preoperative group that was not statistically significant propose that, in patients with ATH, if this UAO condition continues for a long time, may cause left ventricular dysfunction in time. Although there are many studies evaluating the right ventricle functions in children with ATH, there is limited number of studies evaluating LV in literature. For that reason, we believe that larger studies in children especially evaluating the association of ATH with LV functions are warranted. References [1] S.A. Weber, J.C. Montovani, B. Matsubara, J.R. Fioretto, Echocardiographic abnormalities in children with obstructive breathing disorders during sleep,
45
J. Pediatr. (Rio J.) 83 (2007) 518e522. [2] Z. Xu, D.K. Cheuk, S.L. Lee, Clinical evaluation in predicting childhood obstructive sleep apnea, Chest 130 (2006) 1765e1771. [3] S.E. Brietzke, D. Gallagher, The effectiveness of tonsillectomy and adenoidectomy in the treatment of pediatric obstructive sleep apnea/hypopnea syndrome: a meta-analysis, Otolaryngol. Head. Neck Surg. 134 (2006) 979e984. [4] M.P. Major, C. Flores-Mir, P.W. Major, Assessment of lateral cephalometric diagnosis of adenoid hypertrophy and posterior upper airway obstruction: a systematic review, Am. J. Orthod. Dentofac. Orthop. 130 (2006) 700e708. [5] M.K. Park, R.G. Troxler, Pulmonary Hypertension in Pediatric Cardiology for Practitioners, fourth ed., Mosby Inc., St Louis, MO, 2002, pp. 417e426. [6] D. Duman, B. Naiboglu, H.S. Esen, S.Z. Toros, R. Demirtunc, Impaired right ventricular function in adenotonsillar hypertrophy, Int. J. Cardiovasc. Imaging 24 (3) (2008) 261e267. [7] M.D. Yilmaz, E. Onrat, A. Altuntas¸, et al., The effects of tonsillectomy and adenoidectomy on pulmonary arterial pressure in children, Am. J. Otolaryngol. Head Neck Med. Surg. 26 (1) (2005) 18e21. [8] M.C. Petrie, L. Caruana, C. Berry, J.J. McMurray, “Diastolic heart failure” or heart failure caused by subtle left ventricular systolic dysfunction? Heart 87 (2002) 29e31. [9] T. Kukulski, L. Hubbert, M. Arnold, B. Wranne, L. Hatle, G.R. Sutherland, Normal regional right ventricular function and its change with age: a Doppler myocardial imaging study, J. Am. Soc. Echocardiogr. 13 (2000) 194e204. [10] M. Butt, G. Dwivedi, A. Shantsila, O.A. Khair, G.Y. Lip, Left ventricular systolic and diastolic function in obstructive sleep apnea: impact of continuous positive airway pressure therapy, Circ. Heart Fail. 5 (2012) 226e233. [11] A. Romero-Corral, V.K. Somers, P.A. Pellikka, E.J. Olson, K.R. Bailey, J. Korinek, et al., Decreased right and left ventricular myocardial performance in obstructive sleep apnea, Chest 132 (2007) 1863e1870. [12] S.H. Kim, G.Y. Cho, C. Shin, H.E. Lim, Y.H. Kim, W.H. Song, et al., Impact of obstructive sleep apnea on left ventricular diastolic function, Am. J. Cardiol. 101 (2008) 1663e1668. [13] L. Brodsky, Tonsillitis, tonsillectomy and adenoidectomy, in: B.J. Bailey (Ed.), Head and Neck Surgery-Otolaryngology, Lippincott, Philadelphia, 1993, pp. 833e847. [14] M. Greenfeld, R. Tauman, A. DeRowe, Y. Sivan, Obstructive sleep apnea syndrome due to adenotonsillar hypertrophy in infants, Int. J. Pediatr. Otorhinolaryngol. 67 (2003) 1055e1060. [15] N.B. Schiller, P.M. Shah, M. Crawford, A. DeMaria, R. Devereux, H. Feigenbaum, et al., Recommendations for quantification of left ventricle by twodimensional echocardiography. American society of echocardiography committee on standards, subcommitee on quatification of two-dimensional echocardiograms, J. Am. Soc. Echocardiogr. 2 (1989) 358e367. [16] A. Dabestani, G. Mahan, J.M. Gardin, K. Takenaka, C. Burn, A. Allfie, et al., Evaluation of pulmonary artery pressure and resistance by pulsed Doppler echocardiography, Am. J. Cardiol. 59 (1987) 662e668. [17] G. Mahan, A. Dabestani, J. Gardin, et al., Estimation of pulmonary artery pressure by pulsed Doppler echocardiography, Circulation 68 (suppl 3) (1983). III-367. [18] A. Kitabatake, M. Inoue, M. Asao, et al., Noninvasive evaluation of pulmonary hypertension by a pulsed Doppler technique, Circulation 68 (1983) 302e309. [19] R.M. Lang, M. Bierig, R.B. Devereux, et al., Chamber quantification writing group; american society of echocar-diography’s guidelines and standards committee; european association of echocardiography. Recommendations for chamber quantification: a report from the american society of Echocardiography's guidelines and standards committee and the chamber quantification writing group, developed in conjunction with the european association of echocardiography, a branch of the european society of cardiology, J. Am. Soc. Echocardiogr. 18 (2005) 1440e1463. [20] L.G. Rudski, W.W. Lai, J. Afilalo, et al., Guidelines for the echocardiographic assessment of the right heart in adults: a report from the american society of echocardiography endorsed by the european association of echocardiography, a registered branch of the european society of cardiology, and the canadian society of echocardiography, J. Am. Soc. Echocardiogr. 23 (2010) 685e713. [21] A.M. Levy, B.S. Tabakin, J.S. Hanson, R.M. Narkewicz, Hypertrophied adenoids causing pulmonary hypertension and severe cardiac failure, N. Engl. J. Med. 277 (1967) 506e511. [22] A. Widlitz, R.J. Barst, Pulmonary arterial hypertension in children, Eur. Respir. J. 21 (2003) 155e176. € [23] M. Çetin, M. Yılmaz, S. Ozen, N. Bozan, S¸. Cos¸kun, Assessment of pulmonary artery pressure and right ventricular function in children with adenotonsillar hypertrophy using different parameters, Int. J. Pediatr. Otorhinolaryngol. 78 (11) (2014) 1837e1842. [24] V.F. Martha, S. Moreira Jda, A.S. Martha, F.J. Velho, R.G. Eick, S.C. Goncalves, Reversal of pulmonary hypertension in children after adenoidectomy or adenotonsillectomy, Int. J. Pediatr. Otorhinolaryngol. 77 (2) (2013) 237e240. [25] S. Koc, M. Aytekin, N. Kalay, M. Ozcetin, T. Burucu, K. Ozbek, A. Celik, H. Kadi, S. Gulturk, F. Koc, The effect of adenotonsillectomy on right ventricle function and pulmonary artery pressure in children with adenotonsillar hypertrophy, Int. J. Pediatr. Otorhinolaryngol. 76 (1) (2012) 45e48. [26] Y. Jabbari Moghaddam, S.G. Bavil, K. Abavisani, Do pre-adenotonsillectomy echocardiographic findings change postoperatively in children with severe adenotonsillar hypertrophy, J. Saudi Heart Assoc. 23 (1) (2011) 31e35. [27] F.T. Orji, F.A. Ujunwa, N.G. Umedum, O. Ukaegbe, The impact of
46
[28] [29] [30]
[31]
[32]
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46 adenotonsillectomy on pulmonary arterial pressure in West African children with adenotonsillar hypertrophy, Int. J. Pediatr. Otorhinolaryngol. 92 (2017) 151e155. J.P. Bounhoure, M. Galinier, A. Didier, P. Leophonte, Sleep apnea syndromes and cardiovascular disease, Bull. Acad. Natl. Med. 189 (2005) 445e459. J.W. Weiss, S.H. Launois, A. Anand, E. Garpestad, Cardiovascular morbidity in obstructive sleep apnea, Prog. Cardiovasc Dis. 41 (1999) 367e376. T. Shiomi, C. Guilleminault, R. Stoohs, I. Schnittger, Leftwardshift of the interventricular septum and pulsus paradoxusin obstructive sleep apnea syndrome, Chest 100 (1991) 894e902. R.S. Amin, T.R. Kimball, J.A. Bean, J.L. Jeffries, J.P. Willging, R.T. Cotton, S.A. Witt, B.J. Glascock, S.R. Daniels, Left ventricular hypertrophy and abnormal ventricular geometry in children and adolescents with obstructive sleep apnea, Am. J. Respir. Crit. Care Med. 165 (10) (2002) 1395e1399. € rür, O. Do €ven, M. Unal, N. Akkus¸, C. Ozcan, Preoperative and postK. Go operative cardiac and clinical findings of patients with adenotonsillar
hypertrophy, Int. J. Pediatr. Otorhinolaryngol. 59 (2001) 41e46. [33] A.G. Kaditis, E.I. Alexopoulos, M. Dalapascha, K. Papageorgiou, E. Kostadima, D.G. Kaditis, K. Gourgoulianis, E. Zakynthinos, Cardiac systolic function in Greek children with obstructive sleep-disordered breathing, Sleep. Med. 11 (4) (2010) 406e412. [34] G. Attia, M.A. Ahmad, A.B. Saleh, A. Elsharkawy, Impact of obstructive sleep apnea on global myocardial perfor-mance in children assessed by tissue Doppler imaging, Pediatr. Cardiol. 31 (2010) 1025e1036. [35] A. Cincin, E. Sakalli, E.M. Bakirci, R. Dizman, Relationship between obstructive sleep apnea-specific symptoms and cardiac function before and after adenotonsillectomy in children with adenotonsillar hypertrophy, Int. J. Pediatr. Otorhinolaryngol. 78 (8) (2014) 1281e1287. [36] M. Vogel, G. Derrick, P.A. White, S. Cullen, H. Aichner, J. Deanfield, A.N. Redington, Systemic ventricular function in patients with tranposition of the great arteries after atrial repair. A tissue Doppler and conductance catheter study, J. Am. Coll. Cardiol. 43 (2004) 100e106.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: http://www.ijporlonline.com/
The effects of adenotonsillar hypertrophy corrective surgery on left ventricular functions and pulmonary artery pressure in children Mecnun Çetin a, *, Nazım Bozan b a b
Department of Pediatric Cardiology, Yuzuncu Yil University, Van, Turkey Department of Otolaryngology, Yuzuncu Yil University, Van, Turkey
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 July 2017 Accepted 20 July 2017 Available online 22 July 2017
Objective: Comparison of left ventricular functions in preoperative and postoperative periods of children with adenotonsillar hypertrophy (ATH) who have findings of upper airway obstruction (UAO), using echocardiographic parameters. Methods: Thirty children who were diagnosed with UAO due to ATH, and who have undergone adenoidectomy/adenotonsillectomy and 30 healthy children, between 2 and 11 years of age, were included in the study. Patient group was evaluated by the pulsed wave tissue Doppler echocardiography, as well as with conventional echocardiography, before and 6 months after the operation. Results: Of 30 children in study group, 18 (60%) had adenotonsillectomy and 12 (40%) had adenoidectomy. The differences between groups regarding myocardial performance index (MPI) was not statistically significant (p ¼ 0.847). There was not any statistically significant difference between groups in terms of mitral isovolemic acceleration (MIVA) (2.28 ± 0.67, 2.24 ± 0.55, 2.23 ± 0.49; p ¼ 0.943, respectively). Interventricular septum diameter (IVSD) was significantly higher in preoperative group than postoperative and control groups (3.68 ± 0.52, 3.50 ± 0.40, 3.38 ± 0.60; p ¼ 0.028, respectively). Pulmonary acceleration time (PAcT) was found to be significantly lower in preoperative group compared to postoperative and control groups (107.64 ± 16.60, 119.52 ± 15.95, 120.47 ± 16.19; p ¼ 0.004, respectively). Mean pulmonary arterial pressure (mPAP) was significantly higher in preoperative group than postoperative and control groups (30.58 ± 8.11, 25.23 ± 9.07, 25.00 ± 6.52; p ¼ 0.002, respectively). In postoperative group mPAP was found to be similar to the control group. Conclusions: Clinical or subclinical left ventricle (LV) dysfunction in children with ATH who have findings of UAO was not determined while mean pulmonary arterial pressure was significantly higher compared with the control cases. Besides early adenotonsillectomy is a beneficial treatment option for these patients. © 2017 Elsevier B.V. All rights reserved.
Keywords: Adenotonsillar hypertrophy (ATH) Left ventricle (LV) Tissue doppler echocardiography
1. Introduction Upper airway obstruction (UAO) during sleep comprises a large spectrum of symptoms varying from night time snoring to the obstructive sleep apnea-hypopnea syndrome. The most common symptoms defined are the snoring, respiratory pauses, difficulty in breathing, agitated sleep and nocturnal diaphoresis [1]. Adenotonsillar hypertrophy (ATH), the excessive lymphoid tissue proliferation on adenoids and tonsils, is the most common cause of upper air-way obstruction in pediatric population [2e4].
* Corresponding author. Tel.: þ90 432 215 0473; fax: þ90 432 216 83 52. E-mail address: [email protected] (M. Çetin). http://dx.doi.org/10.1016/j.ijporl.2017.07.027 0165-5876/© 2017 Elsevier B.V. All rights reserved.
Severe UAO can result in chronic alveolar hypoventilation, which may cause hypoxemic pulmonary vasoconstriction and the resulting rise in pulmonary vascular resistance and pulmonary arterial pressure (PAP). Dilatation and hypertrophy of the right side of the heart and subsequent right ventricular dysfunction are the end results of persistent pulmonary vascular resistance [5,6]. Early recognition of ventricular dysfunction is important in prevention of further progression to heart failure and even death and also in decision of requirement of surgical treatment [7,8]. Recently, tissue Doppler echocardiography (TDI) has been defined as a reliable and accurate technique in evaluation of global and regional ventricular functions [9]. Although the data in literature is conflicting, majority of studies suggest that severe UAO contributes to the development of left
42
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
ventricular systolic and diastolic dysfunctions and subsequently heart failure [10]. However, the exact pathophysiological mechanisms linking UAO to cardiovascular disease or the long-term impacts of UOA on cardiovascular system were not defined clearly, yet. Even though there are many studies about the effects of ATH on left ventricle functions in adults [11,12], and there are many studies in children dealing with the effects of ATH on right ventricle; the data about the association of ATH with left ventricle functions in children is limited. The objective of this study was to evaluate the left ventricle (LV) functions in children with ATH, by means of TDI, and to determine the effects of adenotonsillectomy on LV functions by comparing pre- and post-operative data. 2. Methods The study protocol was approved by the University of Yuzuncu Yil Ethics Committee. Informed consent was obtained from parents of the participants. Thirty patients (17 male, 13 female, mean age 5.8 ± 3.0 years) with history and physical examination findings suggestive of UAO, who have undergone adenoidectomy/adenotonsillectomy due to stage III or stage IV adenoid and/or ATH were included in the study. In control group, there were 30 healthy children (15 male, 15 female, mean age 5.9 ± 2.1 years) who were admitted to pediatric cardiology outpatient clinic with murmur, syncope, or chest pain and whose echocardiographic evaluations revealed no pathologic findings. The participants were selected consecutively. A questionnaire was applied to the study group with the purpose of determining whether there were symptoms related to upper respiratory tract obstruction (snoring, respiratory arrest during sleep, open mouth, sleeping, suddenly waking up at night, nocturnal diuresis, mouth open navigation and sleepiness during the day) (Table 3). Parents were asked to answer the questions in questionnaire. Answers such as always, frequently and yes were considered as positive and the ones like sometimes, never, and no were considered as negative responses. Exclusion criteria were as follows: presence of additional pathologies leading to UAO other than ATH, heart disease with congenital origin or secondary to another disease, primary pulmonary hypertension, any systemic diseases, obesity, craniofacial anomaly, and genetic syndrome or inability to obtain informed consent from family. Detailed histories of the patients were obtained and comprehensive physical examination including height, weight, and arterial blood pressure measurements were performed in all participants. Degree of tonsillar hypertrophy of the study group was determined with paranasal sinus radiographs and clinical findings, according to the Brodsky scale, regarding the degree of oropharyngeal obstruction due to palatine tonsils [13]. Examination of adenoids was performed by fibreoptic endoscopy. According to this evaluation, percentage of obstruction of the passage by adenoids was determined and staging was performed [14]. Conventional Doppler echocardiography (CDE) and TDI values for all patients were recorded. Study group was evaluated by echocardiography in preoperative period and on 6th month after operation.
2.2. Echocardiography Echocardiography was performed on the left lateral decubitus and supine positions with an ultrasound machine Vivid 6S (GEVingmed Ultrasound AS, Horten, Norway) and 3S-RS (3.5 Mhz) probe. Averages of three consecutive cycles were measured for all echocardiographic data. Images were obtained from parasternal and apical positions using 2D, M-mode and Doppler echocardiographic techniques. M-mode echocardiographic measurements were performed according to standards outlined by the American Society of Echocardiography [15]. The following variables were measured: interventricular septum diameter (IVSD), left ventricle fractional shorting (LVFS), left ventricle (LV) diameter and LV posterior wall thickness (LVpWD). IVSD and LVpWD were measured at the end of diastole in parasternal long axis. Left ventricular end-diastolic (LVedD) and end-systolic diameter (LVesD) were measured at the end of systole and diastole in parasternal long axis. LVFS was calculated as the percentage decrease of LV systolic diameter to the diastolic diameter. The pulmonary acceleration time (PAcT), pulmonary peak velocity (PPV) and pulmonary ejection time (PET) were obtained using the pulse wave Doppler with the pulse wave sample volume placed within the RV outflow tract. PET was measured as the time from onset to completion of systolic pulmonary flow. PAcT is the time interval between the onset of the systolic velocity and the peak systolic velocity [16]. Using this measurement, the mean pulmonary artery pressure (mPAP) was calculated by the equation (Mahan formula): mPAP ¼ 79e (0.45 PAcT) [17,18]. TDI was recorded from the apical 4C view with the pulse wave Doppler sample volume placed on the mitral lateral annulus. Peak systolic (Sm) velocity, peak early (Em), the deceleration time (DT) of Em wave and peak late (Am) diastolic myocardial annular velocity, isovolemic relaxation time (IVRT), and isovolemic contraction time (IVCT) were measured. Myocardial performance index (MPI) was calculated with the Tei index formula. Mitral isovolemic acceleration (MIVA) for the LV was calculated by dividing the isovolemic contraction peak velocity by the time interval between the onset of this wave and its peak velocity [19,20] (Fig. 1). Examinations were performed by single experienced pediatric cardiologists.
2.1. Operative management Preoperative routine anesthetic evaluations were including blood tests and chest X-ray. All children were operated as inpatient and under general anesthesia. Adenoidectomy in 12 patients and adenotonsillectomy in 18 patients were carried out by curettage and cold dissection methods. Postoperative period care was uneventful in all children. The average period of hospital stay was two days.
Fig. 1. Calculation of left ventricular MPI and MIVA with TDI. MIVA, mitral isovolumic acceleration; IVV, isovolumic contraction peak velocity; AcT, acceleration time; Sm, systolic myocardial velocity; Em, early diastolic myocardial velocity; Am, late diastolic myocardial velocity; IVRT, isovolumic relaxation time; IVCT, isovolumic contraction time; ET, ejection time; MPI, myocardial performance index.
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
43
Table 1 General characteristics of the study population (mean ± SD). SBP, systolic blood pressure; DBP, diastolic blood pressure.
Age (years) Sex (male/female) Weight (kg) Height (cm) SBP (mmHg) DBP (mmHg) Heart rate (beats/min)
Preop (n ¼ 30)
Postop (n ¼ 30)
Control (n ¼ 30)
P
5.8 þ 3.0 17/13 22.4 þ 7.1 114 þ 13 93.0 þ 7.2 57.7 þ 7.1 96.2 þ 9.5
5.8 þ 3.0 17/13 22.4 þ 7.1 114 þ 13 96.1 þ 10.0 59.4 þ 9.0 93.8 þ 13.1
5.9 þ 2.1 15/15 23.5 þ 5.9 115 þ 10 91.4 þ 8.8 55.4 þ 9.4 95.4 þ 10.2
0.853 0.545 0.723 0.907 0.110 0.213 0.691
2.3. Statistical analysis Statistical analyses were performed with the SPSS (ver: 15.0) statistical program. Descriptive statistics for the continuous variables were presented as mean ± standard deviation; minimum and maximum values while count and percentages for categorical variables. One-way ANOVA was used to compare the group means. Duncan multiple comparison test was also used to identify different group means followed by ANOVA. In addition, chi-square test was performed to determine the relationship between categorical variables. Statistical significance level was considered as 0.05. 3. Results Seventeen of 30 patients in the study group (56.6%) and 15 of the 30 patients in the control group (50%) were male. Age, gender, weight, height, blood pressure and heart rate were not statistically significantly different between 2 groups (Table 1). Twelve patients (40%) in study group had adenoidectomy while 18 (60%) were operated for adenotonsillectomy (Table 2). When the symptoms of patients were investigated; during preoperative period all 30 patients in the study group were having snoring symptoms. Snoring complaint which was present in all of 30 patients disappeared in 23 of them, postoperatively. Of 22 patients with ATH, 20 reported that their complaints improved. As a result, all complaints of the patients revealed statistically significant differences between preoperative and postoperative periods (Table 3). 3.1. Echocardiographic data In the assessment made by M-mode echocardiography, IVSD
Table 2 The degree of adenoid and tonsillar hypertrophy of the study group. Type of operation
Grade II n (%)
Grade III n (%)
Grade IV n (%)
Total n (%)
Tonsillectomy Adenoidectomy
3 (16.6) 0 (0)
12 (66.8) 20 (66.7)
3 (16.6) 10 (33.3)
18 (100) 30 (100)
was significantly higher in preoperative group than postoperative and control groups (3.68 ± 0.52, 3.50 ± 0.40, 3.38 ± 0.60; p ¼ 0.028, respectively). The difference between postoperative and control groups was not significant (p > 0.05). There was not any statistically significant difference between the groups, in terms of LVpWD, LVesD, LVedD and LVFS (Table 4). PAcT obtained by CDE was significantly lower in preoperative group (p ¼ 0.004). Also mPAP was significantly higher in preoperative group compared to other 2 groups (p ¼ 0.002) (Fig. 2). Any significant difference was not detected between postoperative and control groups regarding all variables (Table 4). In evaluation of LV TDI; There was not any statistically significant difference between the groups, in terms of MIVA (2.28 ± 0.67, 2.24 ± 0.55, 2.23 ± 0.49; p ¼ 0.943, respectively). The differences in MPI values in preoperative, postoperative and control groups were not statistically significant (0.38 ± 0.07, 0.35 ± 0.06, 0.36 ± 0.06; p ¼ 0.847, respectively). There was also not any significant difference between groups, in terms of other variables (p > 0.05) (Table 5). 4. Discussion The data about the LV functions in children with ATH is limited. In this study we evaluated the effects of ATH in children who have findings of UAO on pulmonary system and LV functions by CDE and TDI and we have determined that after adenotonsillectomy the symptoms of patients significantly improved. Regarding the echocardiographic data, we did not determine a significant difference between groups in terms of LV functions including LVpWD, LVedD, LVesD or LVFS; however IVSD was significantly higher together with the mPAP in preoperative group. The most common cause of UAO in children is the ATH. The development of pulmonary hypertension and heart dysfunction in patients with chronic UAO is complex. Respiratory acidosis induced by hypoxemia and hypercarbia is the main mediator of pulmonary vasoconstriction that can lead to reversible or irreversible chronic changes in the pulmonary vasculature. Moreover, various neurohumoral factors produced in response to respiratory distress may additionally promote pulmonary hypertension, right ventricular dysfunction, and consequent impairment of systemic cardiac output [2,21,22].
Table 3 The patient's preoperative and postoperative symptoms. Preoperative
Snoring Stop breathing during sleep Open mouth breathing Suddenly waking up at night Enuresis Open mouth during daytime Daytime sleepiness
Postoperative
P
Yes n (%)
No n (%)
Yes n (%)
No n (%)
30 (100) 22 (73.4) 28 (93.4) 12 (40) 4 (13.3) 17 (56.6) 5 (16.6)
0 (0) 8 (26.6) 2 (6.6) 18 (60) 26 (86.7) 13 (43.4) 25 (83.4)
7 2 6 0 1 3 0
23 28 24 30 29 27 30
(23.3) (6.6) (20) (0) (3.3) (10) (0)
(76.7) (93.4) (80) (100) (96.7) (90) (100)
<0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05
44
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
Table 4 Left ventricular 2D echocardiographic measurements of groups, and pulmonary flow evaluations and mPAP values obtained by conventional dopppler echocardiography (mean ± SD). LVpWD, left ventricle posterior wall diameter; LVedD, left ventricle end-diastolik diameter; LVesD, left ventricle end-sistolik diameter; LVFS, fractional shorting of left ventricle; IVSD, interventriculare septum diamater. PET, pulmonary ejection time; PPV, pulmoner peak velocity; PAcT, acceleration time; mPAP, mean pulmonary artery pressure.
LVpWD (mm) LVedD (mm) LVesD (mm) LVFS IVSD (mm) PET (msn) PAcT (msn) PPV (m/sn) mPAP (mmHg)
Preop (n ¼ 30)
Postop (n ¼ 30)
Control (n ¼ 30)
P
3.66 ± 0.4 34.6 ± 2.9 24.3 ± 3.8 30.77 ± 3.5 3.68 ± 0.52a 267.9 ± 21.2 107.6 ± 16.6b 0.98 ± 0.13 30.58 ± 8.11a
3.81 ± 0.4 34.7 ± 3.6 23.4 ± 3.4 32.56 ± 5.2 3.50 ± 0.40a 278.2 ± 19.6 119.5 ± 15.9b 1.05 ± 0.09 25.23 ± 9.07b
3.71 ± 0.7 35.2 ± 3.9 23.3 ± 3.5 34.09 ± 2.9 3.38 ± 0.60b 269.9 ± 12.4 120.4 ± 16.1a 1.01 ± 0.13 25.00 ± 6.52b
0.584 0.772 0.519 0.123 0.028 0.076 0.004 0.130 0.002
Table 5 LV TDI values of groups (mean ± SD). Sm, systolic myocardial velocity; Em, early diastolic myocardial velocity; Am, late diastolic myocardial velocity; DT, deceleration time; IVRT, isovolumic relaxation time; IVCT, isovolumic contraction time; ET, ejection time; MPI, myocardial performance index; MIVA, mitral isovolumic acceleration.
Sm (cm/sn) Em (cm/sn) Am (cm/sn) Em/Am DT (msn) IVRT (msn) IVCT (msn) ET (msn) MPI MIVA (m/sn2)
Preop (n ¼ 30)
Postop (n ¼ 30)
Control (n ¼ 30)
P
8.91 ± 2.80 17.55 ± 3.08 6.75 ± 1.89 2.60 ± 0.85 75.42 ± 13.27 42.45 ± 11.34 58.64 ± 16.46 265.6 ± 20.2 0.38 ± 0.07 2.28 ± 0.67
9.44 ± 0.41 17.06 ± 2.56 6.46 ± 1.65 2.98 ± 0.68 76.11 ± 11.74 42.09 ± 9.60 53.45 ± 8.47 274.5 ± 22.1 0.35 ± 0.06 2.24 ± 0.55
8.93 ± 1.32 18.42 ± 2.81 6.42 ± 1.53 2.71 ± 0.63 74.09 ± 13.66 43.38 ± 9.16 52.09 ± 11.68 268.2 ± 15.0 0.36 ± 0.06 2.23 ± 0.49
0.791 0.174 0.726 0.127 0.580 0.877 0.340 0.196 0.847 0.943
a,b
; The different lower cases represent statistically significant difference.
Until the rapid onset of severe cardiac decompensation occurs, progressive pulmonary hypertension may cause minimal symptoms. In that aspect, for the decision of early surgical approach detection of subclinical cardiac impairment is crucial. Eventually, a reliable, noninvasive, and simple method is desirable for the decision of early surgical treatment. Elevated PAP values associated with ATH in children were reported before those were mostly reversible after adenotonsillectomy [23e25]. Jabbari et al. evaluated the changes of preadentonsillectomy echocardiographic findings after adenotonsillectomy and reported that severe chronic ATH caused higher tricuspid regurgitation pressure and mean pulmonary arterial pressure that were improved after adenotonsillectomy [26]. Recently, Orji et al. reported a significant decrease in mPAP values after adenotonsillectomy in 39 children with ATH. They also reported that, in 14 of 17 children with pulmonary hypertension, mPAP decreased to normal range 6 weeks after operation [27]. In our study, in preoperative group PAcT value, which is inversely correlated with mPAP, was found to be significantly lower compared to postoperative and control group. The PAcT values at 6 month after operation and control group was found to be similar. In the same way, mPAP was significantly higher in preoperative group. In postoperative group mPAP was similar to control group.
Children with obstructive respiratory disorders during sleep are exposed to repeated hypopnea and apnea periods. Hypercapnia and hypoxemia that take place during apnea periods provoke respiratory acidosis and resulting vasoconstriction of the pulmonary artery. Throughout sleeping, decubitus horizontal position and intra-thoracic pressure which becomes more negative due to respiratory effort against the obstruction also increase venous return to the right-hand cardiac chambers, in addition to increased pulmonary resistance. Right ventricle volume increases with an increase in venous return that alters the position of interventricular septum through left ventricle which in turn decreases the left ventricle compliance and end-disatolic volume. The augmented negativity of intra-thoracic pressure also alters the balance between extra- and intra-cardiac pressures and increases the transmural pressure of left ventricle. With the effects of negative intrathoracic pressure, the blood flow through thoracic aorta becomes more difficult increasing the left ventricle afterload. Those alterations can lead to ventricular global dysfunction [1,28e30]. There are some studies in literature evaluating left ventricle functions in children with ATH or OSAS. Amin et al. reported an abnormal LV geometry in 15% of 19 children with habitual snoring and in 39% of 28 children with OSAS, and OSAS was associated with €rür et al. on increased LV mass in children [31]. In a study of Go children with ATH, LVedD and IVSD values were reported to be significantly higher in preoperative group [32]. In another study in
Fig. 2. Distribution of mPAP between groups, Statistically significant difference was determined between groups, p < 0.05.
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46
children with moderate-severe OSAS, left ventricular ejection fraction and LVFS were determined to be lower compared with patients having mild OSAS or primary snoring and the authors defined a negative correlation between LV systolic functions and the degree of UAO [33]. In our study we did not determine a significant difference between groups regarding LVpWD, LVedD, LVesD or LVFS. However, IVSD showed a significant increase in preoperative group compared with control group and although there was a gradual decrease in IVSD in postoperative group compared with the preoperative values. We believe that, this increase in IVSD was due to the RV hypertrophy secondary to the increased pressure in pulmonary system. In a study of Attia et al. on children with OSAS, preoperative MPI value was defined to be significantly decreased in postoperative period and in patients with OSAS secondary to ATH, subclinical alterations in LV were determined with DDI [34]. In another study on children with ATH, DT determined on mitral valve was elongated in patient group compared with the control group which also normalized after adenotonsillectomy and the cause of this elongation was defined as diastolic dysfunction in LV [32]. Cincin et al. reported that, both the LV and RV MPI significantly improved after surgery for ATH [35]. In our study, contrary with the literature, there was not any statistically significant difference between groups regarding systolic and diastolic LV measurements obtained by DDE. Although IVCT and MPI were longer in preoperative group, the differences were not statistically significant. With those findings, at least at that level, we did not determine left ventricular systolic or diastolic dysfunction in study group. The IVA evaluates myocardial motion during the isovolumetric contraction period and it has been validated as a sensitive noninvasive index of LV and RV. The rate of myocardial acceleration during the isovolemic period has been described to correlate with intrinsic myocardial contractility and is thought to be relatively independent of loading conditions [36]. We did not determine any alterations regarding MIVA in patients with ATH in this study. The main limitation of this study is the lack of polysomnographic evaluations. However, it is not feasible to perform polysomnographic evaluations in children and moreover this study is not evaluating the patients with ATH or obstructive sleep apnea; instead we have investigated the patients with the symptoms of upper airway obstruction. In our study, among patients with ATH that were considered to have UAO, significant benefits of adenotonsillectomy were observed based on symptoms. Moreover, with conventional echocardiography, we determined that in patients with ATH pulmonary arterial pressure was higher in preoperative period and improved to normal values with adenotonsillectomy. However, in this study evaluating LV with TDI, contrary with the literature, we did not determine any findings of clinical or subclinical left ventricular dysfunction. In the light of these data, we believe that left ventricular dysfunction does not develop in a short time period in childhood as suggested before. The increased MPI values determined in preoperative group that was not statistically significant propose that, in patients with ATH, if this UAO condition continues for a long time, may cause left ventricular dysfunction in time. Although there are many studies evaluating the right ventricle functions in children with ATH, there is limited number of studies evaluating LV in literature. For that reason, we believe that larger studies in children especially evaluating the association of ATH with LV functions are warranted. References [1] S.A. Weber, J.C. Montovani, B. Matsubara, J.R. Fioretto, Echocardiographic abnormalities in children with obstructive breathing disorders during sleep,
45
J. Pediatr. (Rio J.) 83 (2007) 518e522. [2] Z. Xu, D.K. Cheuk, S.L. Lee, Clinical evaluation in predicting childhood obstructive sleep apnea, Chest 130 (2006) 1765e1771. [3] S.E. Brietzke, D. Gallagher, The effectiveness of tonsillectomy and adenoidectomy in the treatment of pediatric obstructive sleep apnea/hypopnea syndrome: a meta-analysis, Otolaryngol. Head. Neck Surg. 134 (2006) 979e984. [4] M.P. Major, C. Flores-Mir, P.W. Major, Assessment of lateral cephalometric diagnosis of adenoid hypertrophy and posterior upper airway obstruction: a systematic review, Am. J. Orthod. Dentofac. Orthop. 130 (2006) 700e708. [5] M.K. Park, R.G. Troxler, Pulmonary Hypertension in Pediatric Cardiology for Practitioners, fourth ed., Mosby Inc., St Louis, MO, 2002, pp. 417e426. [6] D. Duman, B. Naiboglu, H.S. Esen, S.Z. Toros, R. Demirtunc, Impaired right ventricular function in adenotonsillar hypertrophy, Int. J. Cardiovasc. Imaging 24 (3) (2008) 261e267. [7] M.D. Yilmaz, E. Onrat, A. Altuntas¸, et al., The effects of tonsillectomy and adenoidectomy on pulmonary arterial pressure in children, Am. J. Otolaryngol. Head Neck Med. Surg. 26 (1) (2005) 18e21. [8] M.C. Petrie, L. Caruana, C. Berry, J.J. McMurray, “Diastolic heart failure” or heart failure caused by subtle left ventricular systolic dysfunction? Heart 87 (2002) 29e31. [9] T. Kukulski, L. Hubbert, M. Arnold, B. Wranne, L. Hatle, G.R. Sutherland, Normal regional right ventricular function and its change with age: a Doppler myocardial imaging study, J. Am. Soc. Echocardiogr. 13 (2000) 194e204. [10] M. Butt, G. Dwivedi, A. Shantsila, O.A. Khair, G.Y. Lip, Left ventricular systolic and diastolic function in obstructive sleep apnea: impact of continuous positive airway pressure therapy, Circ. Heart Fail. 5 (2012) 226e233. [11] A. Romero-Corral, V.K. Somers, P.A. Pellikka, E.J. Olson, K.R. Bailey, J. Korinek, et al., Decreased right and left ventricular myocardial performance in obstructive sleep apnea, Chest 132 (2007) 1863e1870. [12] S.H. Kim, G.Y. Cho, C. Shin, H.E. Lim, Y.H. Kim, W.H. Song, et al., Impact of obstructive sleep apnea on left ventricular diastolic function, Am. J. Cardiol. 101 (2008) 1663e1668. [13] L. Brodsky, Tonsillitis, tonsillectomy and adenoidectomy, in: B.J. Bailey (Ed.), Head and Neck Surgery-Otolaryngology, Lippincott, Philadelphia, 1993, pp. 833e847. [14] M. Greenfeld, R. Tauman, A. DeRowe, Y. Sivan, Obstructive sleep apnea syndrome due to adenotonsillar hypertrophy in infants, Int. J. Pediatr. Otorhinolaryngol. 67 (2003) 1055e1060. [15] N.B. Schiller, P.M. Shah, M. Crawford, A. DeMaria, R. Devereux, H. Feigenbaum, et al., Recommendations for quantification of left ventricle by twodimensional echocardiography. American society of echocardiography committee on standards, subcommitee on quatification of two-dimensional echocardiograms, J. Am. Soc. Echocardiogr. 2 (1989) 358e367. [16] A. Dabestani, G. Mahan, J.M. Gardin, K. Takenaka, C. Burn, A. Allfie, et al., Evaluation of pulmonary artery pressure and resistance by pulsed Doppler echocardiography, Am. J. Cardiol. 59 (1987) 662e668. [17] G. Mahan, A. Dabestani, J. Gardin, et al., Estimation of pulmonary artery pressure by pulsed Doppler echocardiography, Circulation 68 (suppl 3) (1983). III-367. [18] A. Kitabatake, M. Inoue, M. Asao, et al., Noninvasive evaluation of pulmonary hypertension by a pulsed Doppler technique, Circulation 68 (1983) 302e309. [19] R.M. Lang, M. Bierig, R.B. Devereux, et al., Chamber quantification writing group; american society of echocar-diography’s guidelines and standards committee; european association of echocardiography. Recommendations for chamber quantification: a report from the american society of Echocardiography's guidelines and standards committee and the chamber quantification writing group, developed in conjunction with the european association of echocardiography, a branch of the european society of cardiology, J. Am. Soc. Echocardiogr. 18 (2005) 1440e1463. [20] L.G. Rudski, W.W. Lai, J. Afilalo, et al., Guidelines for the echocardiographic assessment of the right heart in adults: a report from the american society of echocardiography endorsed by the european association of echocardiography, a registered branch of the european society of cardiology, and the canadian society of echocardiography, J. Am. Soc. Echocardiogr. 23 (2010) 685e713. [21] A.M. Levy, B.S. Tabakin, J.S. Hanson, R.M. Narkewicz, Hypertrophied adenoids causing pulmonary hypertension and severe cardiac failure, N. Engl. J. Med. 277 (1967) 506e511. [22] A. Widlitz, R.J. Barst, Pulmonary arterial hypertension in children, Eur. Respir. J. 21 (2003) 155e176. € [23] M. Çetin, M. Yılmaz, S. Ozen, N. Bozan, S¸. Cos¸kun, Assessment of pulmonary artery pressure and right ventricular function in children with adenotonsillar hypertrophy using different parameters, Int. J. Pediatr. Otorhinolaryngol. 78 (11) (2014) 1837e1842. [24] V.F. Martha, S. Moreira Jda, A.S. Martha, F.J. Velho, R.G. Eick, S.C. Goncalves, Reversal of pulmonary hypertension in children after adenoidectomy or adenotonsillectomy, Int. J. Pediatr. Otorhinolaryngol. 77 (2) (2013) 237e240. [25] S. Koc, M. Aytekin, N. Kalay, M. Ozcetin, T. Burucu, K. Ozbek, A. Celik, H. Kadi, S. Gulturk, F. Koc, The effect of adenotonsillectomy on right ventricle function and pulmonary artery pressure in children with adenotonsillar hypertrophy, Int. J. Pediatr. Otorhinolaryngol. 76 (1) (2012) 45e48. [26] Y. Jabbari Moghaddam, S.G. Bavil, K. Abavisani, Do pre-adenotonsillectomy echocardiographic findings change postoperatively in children with severe adenotonsillar hypertrophy, J. Saudi Heart Assoc. 23 (1) (2011) 31e35. [27] F.T. Orji, F.A. Ujunwa, N.G. Umedum, O. Ukaegbe, The impact of
46
[28] [29] [30]
[31]
[32]
M. Çetin, N. Bozan / International Journal of Pediatric Otorhinolaryngology 101 (2017) 41e46 adenotonsillectomy on pulmonary arterial pressure in West African children with adenotonsillar hypertrophy, Int. J. Pediatr. Otorhinolaryngol. 92 (2017) 151e155. J.P. Bounhoure, M. Galinier, A. Didier, P. Leophonte, Sleep apnea syndromes and cardiovascular disease, Bull. Acad. Natl. Med. 189 (2005) 445e459. J.W. Weiss, S.H. Launois, A. Anand, E. Garpestad, Cardiovascular morbidity in obstructive sleep apnea, Prog. Cardiovasc Dis. 41 (1999) 367e376. T. Shiomi, C. Guilleminault, R. Stoohs, I. Schnittger, Leftwardshift of the interventricular septum and pulsus paradoxusin obstructive sleep apnea syndrome, Chest 100 (1991) 894e902. R.S. Amin, T.R. Kimball, J.A. Bean, J.L. Jeffries, J.P. Willging, R.T. Cotton, S.A. Witt, B.J. Glascock, S.R. Daniels, Left ventricular hypertrophy and abnormal ventricular geometry in children and adolescents with obstructive sleep apnea, Am. J. Respir. Crit. Care Med. 165 (10) (2002) 1395e1399. € rür, O. Do €ven, M. Unal, N. Akkus¸, C. Ozcan, Preoperative and postK. Go operative cardiac and clinical findings of patients with adenotonsillar
hypertrophy, Int. J. Pediatr. Otorhinolaryngol. 59 (2001) 41e46. [33] A.G. Kaditis, E.I. Alexopoulos, M. Dalapascha, K. Papageorgiou, E. Kostadima, D.G. Kaditis, K. Gourgoulianis, E. Zakynthinos, Cardiac systolic function in Greek children with obstructive sleep-disordered breathing, Sleep. Med. 11 (4) (2010) 406e412. [34] G. Attia, M.A. Ahmad, A.B. Saleh, A. Elsharkawy, Impact of obstructive sleep apnea on global myocardial perfor-mance in children assessed by tissue Doppler imaging, Pediatr. Cardiol. 31 (2010) 1025e1036. [35] A. Cincin, E. Sakalli, E.M. Bakirci, R. Dizman, Relationship between obstructive sleep apnea-specific symptoms and cardiac function before and after adenotonsillectomy in children with adenotonsillar hypertrophy, Int. J. Pediatr. Otorhinolaryngol. 78 (8) (2014) 1281e1287. [36] M. Vogel, G. Derrick, P.A. White, S. Cullen, H. Aichner, J. Deanfield, A.N. Redington, Systemic ventricular function in patients with tranposition of the great arteries after atrial repair. A tissue Doppler and conductance catheter study, J. Am. Coll. Cardiol. 43 (2004) 100e106.