Materials and methods
1. Subjects
The study was conducted at the Departments of Pediatric Cardiology and Otolaryngology, Konyang University Hospital, from June 2014 to July 2015. Out of 104 children scheduled for adenoidectomy during this period, only children who had OSA caused by ATH were included. Thirty-seven children who underwent echocardiography before and after adenotonsillectomy were included. According to the method of Cohen and Konak [5] and on the Brodsky scale [6], adenoid and tonsil of grades III–IV have been considered to be severe ATH, respectively. We verified OSA using the STOP (snoring-tiredness during the daytime-observed apnea-high blood pressure) questionnaire revised for children. Whether children had adenotonsillectomy was determined by an otolaryngologist and was based on careful examination and detailed medical history [7]. This study was approved by the Institutional Review Board (IRB) of Konyang University Hospital (approval number: 2018-10-015). Informed consent was exempted by the IRB.
2. Echocardiographic examination
All children underwent transthoracic echocardiography conducted by a single pediatric cardiologist before and at least 12 months after adenotonsillectomy. The echocardiogram was obtained in all standard precordial positions via a 3- to 5-MHz transducer of Vivid E9 (General Electric, Oslo, Norway) using 2-dimensional, M-mode, conventional, and tissue Doppler examination according to the American Echocardiography Association guidelines [8]. For each parameter, the average of 5 consecutive cycles was taken.
1) Pulmonary artery pressure
A pulsed wave Doppler of pulmonic forward flow was obtained at the end of expiration, just proximal to the pulmonary valve in the parasternal short axis view. Right ventricular outflow tract (RVOT) acceleration time (AT) was measured from the beginning of the flow to the peak flow velocity (Fig. 1).
We calculated mean pulmonary artery pressure (mPAP) using the formula: mPAP (mmHg)=90−(0.62×ATRVOT) [9,10]. We verified the presence and the maximal velocity of tricuspid regurgitation (TR) for all subjects.
2) Tricuspid annular plane systolic excursion
Tricuspid annular plane systolic excursion (TAPSE) was measured using the M-mode recordings from the apical 4-chamber view with the cursor placed on the free wall side of the tricuspid annulus [11] (Fig. 2) and was presented as a z score adjusted by age [12].
3) Myocardial performance index of right ventricle
Myocardial performance index of right ventricle (RVMPI) was calculated, as described by Tei [13], as the sum of the isovolumetric contraction and isovolumetric relaxation times divided by ejection time. This was performed with TDE (Fig. 3).
Random echocardiography recordings were analyzed to determine the intraobserver variability before the study. Intraobserver variabilities were <5% for all echocardiographic parameters.
3. Statistical analysis
We analyzed data using the PASW Statistics ver. 18.0 (SPSS Inc., Chicago, IL, USA). Continuous variables are presented as mean± standard deviation (median). The significance of the differences in the categorical variables between the groups was analyzed using the chi-square analysis; whereas, the significance of the differences in the continuous variables was evaluated using the Mann-Whitney U test. A P value<0.05 was considered significant.
Results
The clinical characteristics of children before and after adenotonsillectomy are shown in Table 1. Age, weight, height, body surface area, and body mass index (BMI) increased postoperatively, which seems to be caused by a change by age. There was no significant difference between heart rate, BMI, and z score.
The mPAP was normal in children with ATH and there was no difference between pre- and post-T&A results. TR was observed in 17 children before surgery and in 15 patients after surgery. There was no significant difference in the maximal velocity of TR (TRmax) pre- and postsurgically (P=0.78) (Table 2).
The absolute value of TAPSE increased (21.45±0.90 mm vs. 22.30±1.10 mm, P=0.001) after T&A, but this change was noted because of growth. The z score of TAPSE did not differ between pre- and post-T&A (1.19±0.34 vs. 1.24±0.30, P=0.194) (Fig. 4).
The value of RVMPI by TDE significantly improved after surgery (42.18±0.33 vs. 40.08±0.30, P=0.001) (Fig. 5).
Discussion
ATH is the most common cause of upper respiratory tract obstruction and sleep apnea in children [14]. Prolonged upper airway obstruction during sleep leads the significant problems such as hypersomnolence, emotional lability, decreased attention, small stature, enuresis, and cardiopulmonary morbidity [15,16]. T&A has been considered to be the first line of treatment which could improve the quality of life of children for pediatric OSA. Recently, there are many reports that shows marked improvements in right ventricular function, following the surgery in children with ATH.
According to the study by Acar et al. [17] the TAPSE value was lower than normal, and elevated 3 months after T&A in children with ATH. TAPSE, which is easy and fast to perform, provides information about the right ven¬tricular systolic functions. Schmid et al. [18] found that the TAPSE value of patients with severe interstitial lung diseases was significantly lower compared to that of the control group. In our study, the value of TAPSE significantly increased after T&A, but this was a change as children grew up. There was no difference in the TAPSE z value.
We obtained the mPAP using RVOT AT and TR peak velocity before and after T&A. The mPAP of our patients was in normal range even preadenotonsillectomy and was not different significantly pre- and postadenotonsillectomy. However, Koc et al. [2], Görür et al. [19], and Naiboglu et al. [20] cited that mPAP levels was elevated in patients with ATH, the value of mPAP were 31±9 mmHg and 26.3 ±5.4 mmHg, respectively, that is to say, considerable pulmonary hypertension. By contrast there was not any changes of the right ventricular functionin the studies of Pac et al. [21] The cause of this varying result can be explained as follows. The severity of obsturctive sleep apnea-hypopnea syndrome (OSAHS) could not been quantified without polysomnography so there would be a difference in the severity of OSAHS between researchers. The duration of follow-up varied for each study and subjects may be heterogeneous.
Duman et al. [22] also reported that the RVMPI was impaired in pediatric patients with advanced ATH and improved after T&A. Similarly, Attia et al. [23] reported that RV TDE-derived MPI was significantly higher in patients with ATH compared to the control group. We observed that only the value of RV MPI by TDE in has improved children with OSA via T&A.
Evaluation of right ventricular functions by echocardiography is somewhat difficult because of the complex structural geometry of the RV and changes in the contraction pattern. MPI by TDE can be easily measured from the valve annulus with pulsed wave TDE is not affected by cardiac geometry, cardiac rate, blood pressure, or ventricular geometry, as compared to conventional Doppler. SoRV MPI has been found to be clinically useful to define RV function [24]. MPI might be more accurate and reflective of overall cardiac dysfunction than systolic and diastolic measures alone [25]. As a result, this new modality might be more sensitive for detecting subclinical abnormalities [26,27].
In conclusion, we can say that OSA associated with marked ATH might cause RV dysfunction. Based on the results of this study, we deferred that RVMPI by TDE could be the earliest indicator that responds to a change of the RV function in children with OSA.
The follow-up period of our study was longer than that of other investigators. However, the number of subjects was small and the diagnosis of OSA was made without sleep polysomnography.