Evaluation of Pre and Post-operative Pulmonary Artery Pressures in Children with Adenotonsillar Hypertrophy and Correlation with Chronicity: A Prospective Study on 50 Children

Abstract

Children with grade III or IV of adenotonsillar hypertrophy especially of a longer duration, may show cardiovascular changes due to mouth breathing. These changes can be detected on doppler echocardiocardiography which can be used as a screening tool. Fifty paediatric patients of grade 3 and 4 adenotonsillar hypertrophy underwent adenotonsillar resection after a pre-operative work up which included doppler echocardiography to measure pulmonary artery pressures. A post-operative doppler echocardiography was done after three months. 11 children (22%) showed deranged pulmonary artery pressure values with increased mean pulmonary artery pressure (MPAP) and pulmonary artery systolic pressure (PSAP) on preoperative doppler echocardiography, and 2 out of these 11 children had Pulmonary Artery Hypertension. A significant (p < 0.001) improvement was noted in pulmonary artery pressure values (MPAP and PSAP returned to normal) after adenotonsillectomy in 3-month postoperative echocardiography. Also, a statistically significant correlation was obtained between chronicity of symptoms and raised pulmonary artery pressures. Our study concluded that these children with chronic untreated upper airway obstructive symptoms get predisposed to potential cardiac complications. And these grave consequences can be easily prevented by a timely intervention.

Introduction

Adenotonsillar hypertrophy (ATH) is primarily a disease of paediatric age group. Adenoid and tonsil act as the primary defense mechanism against upper airway infections in children until other mechanisms of immunity have not yet developed [1, 2]. As a result, hypertrophy of these structures is a frequent finding which may sometimes lead to obstructive symptoms. Also, the clinical symptoms are more common in a younger age group due to the relatively smaller volume of the nasopharynx and the higher frequency of upper respiratory tract infections [3, 4].

In early stages, ATH is usually asymptomatic. With progression of the disease, patients manifest with chronic mouth breathing, sleep disturbances, nasal obstruction, rhinorrhea, swallowing difficulties, snoring, cough, epistaxis, recurrent sore throat, loss of cravings and halitosis [5]. When obstructive sleep apnea (OSA) develops as a consequence of adenoid hypertrophy, it can cause more severe, long-term morbidity such as failure to thrive, learning difficulties, delayed speech, decreased intelligence quotient, and hyperactivity. Possible cardiovascular impairment consists of elevated diastolic blood pressure, left ventricular hypertrophy, and decreased right ventricular ejection fraction [6, 7].

Upper airway obstruction (UAO) due to ATH disturbs the airflow from the nose, which has a laminar flow pattern, and this impairs the physiologic ventilation of the lungs. Because the usual route of airflow is via the nasal passage, upper airway resistance rises to increase nasal airflow. If sufficient airflow cannot be established by the nasal route, mouth breathing becomes obligatory. During mouth breathing, which causes a turbulent airflow, the intraluminal air pressure cannot reach the appropriate level to keep the nasopharyngeal and oropharyngeal airway open in the supine position. Moreover, the bulk of the tongue displaces backwards by the influence of gravity thereby obstructing the airway. This chain of events results in alveolar hypoventilation, hypoxia, and hypercapnia while asleep [8].

Hypoxemia and hypercapnia induced respiratory acidosis leads to pulmonary artery vasoconstriction. Sustained pulmonary artery vasoconstriction leads to increased pulmonary artery systolic pressure (PASP) [normal PASP = 17–25 mm Hg] and increased mean pulmonary artery pressure (MPAP) [normal MPAP = 15–20 mm Hg]. End stage of these increased pressures culminates into condition of pulmonary arterial hypertension (PAH) [PASP > 35 mm Hg or MPAP > 25 mm Hg]. Prolonged PAH causes right ventricular dilation, followed by eventual cardiac failure and cor pulmonale. Doppler echocardiography is an excellent tool for screening of these cardiovascular changes as suggested by Miman et al. [9].

This study was conducted on 50 paediatric subjects with chronic severe ATH who underwent adenotonsillectomy, with preoperative doppler echocardiography to determine if there is evidence of preclinical cardiovascular changes in the form of raised pulmonary artery pressure following chronic UAO, and its correlation was done with chronicity of symptoms. Reversal of these changes following surgery was also investigated.

Material and Methodology

This study was a prospective cross sectional study conducted to assess the correlation of chronic UAO with development of cardiopulmonary issues and their revocation with timely surgery. The study was carried out in the department of ENT, Government medical college and Rajindra hospital, Patiala on 50 patients of clinically diagnosed cases of ATH.

The study protocol was approved by the Institutional Review Board for Ethical Clearance of Government Medical College and Rajindra Hospital and it was performed in accordance with the Code of Ethics of the World Medical Association according to the Declaration of Helsinki of 1975, as revised in 2000.

Inclusion criteria included 50 children of both sexes, aged between 4 and 14 years, with a history of nasal obstruction and mouth breathing as told by parents, with a grade 3 or 4 adenoid hypertrophy (according to Clemens et al. grading of adenoid hypertrophy - diagnosed endoscopically) and grade 3 or 4 tonsillar hypertrophy (according to Brodsky grading of tonsil hypertrophy- diagnosed clinically on oropharyngeal examination). Exclusion criteria included all other causes of nasal obstruction, congenital heart disease, lung disease, previously diagnosed or detected PAH, any respiratory infection whether lower or upper airway in the past 14 days, had some other syndrome and craniofacial deformity.

After selection of study subjects, all participants parents and guardians were properly informed about the tests that he/she would undergo and a written informed consent was taken. These selected 50 subjects underwent a detailed clinical workup, including a complete ENT history and examination. History was taken by the parents and they were asked to fill the Paediatrics sleep questionnaire for assessment of obstructive symptoms and disordered sleep. Duration of symptoms was especially made note of. Height and weight were checked to calculate the mean body mass index (BMI). Following this, complete oropharyngeal examination with headlight to grade palatine tonsillar hypertrophy was done for each case. Rigid endoscopy first pass to grade adenoid hypertrophy was also carried out in each child.

Using Philips IE33 cardiovascular ultrasound machine, doppler echocardiography was done in the cardiology department by a cardiologist to measure MPAP and PASP. In all patients, doppler echocardiography was performed 1 week before the surgery. MPAP in the range of 15–20 mmHg and PASP in the range of 17–25 mmHg were considered normal. MPAP > 20 mmHg and PASP > 25 mmHg was considered raised, and children with MPAP > 25mmHg and PASP > 35 mmHg were considered to have PAH. The chronicity of symptoms was compared with pulmonary artery pressures.

Following this, all of them were subjected to operative procedure of adenotonsillar resection after relevant blood investigations and pre-anesthetic checkup. The patients underwent adenotonsillectomy while lying supine, under general anesthesia, with orotracheal intubation. Both adenoidectomy and tonsillectomy were performed using the conventional cold steel techniques.

Post operatively, the parents were again asked to fill the Paediatrics sleep questionnaire to assess improvement in obstructive symptoms. All study subjects were followed up periodically with nasopharyngeal and oropharyngeal examination. A post-operative doppler echocardiography was done in all children after 3 months to evaluate the pulmonary artery pressure (MPAP and PASP). The cardiologist was blinded to the operative status of these children as well as to the fact that they were part of a study to eliminate bias.

Pre- and post-operative data on symptoms and pulmonary artery pressures was compared and analyzed statistically using Statistical Package for the Social Sciences version 22.0 software for Windows (SPSS Inc, Chicago, Illinois, USA). Descriptive statistics was done for all data and were reported in terms of mean, S.D and percentages. Statistical significance was taken as p < 0.05.

Results

In this study, out of 50 subjects, 32 were males (64%) and 18 were females (36%). The mean age in the study was 8.86 ± 3.02 years with a range of 4–14 years. Maximum patients were in the age group of 8–12 years (42%) followed by 4–8 years (34%) and 12–14 years (24%). The BMI in our study was 18.22 kg/m² ranging from 15.4 to 30.6 kg/m². [Table 1]

Table 1.

Patient Demographics

Age
Mean	8.86 ± 3.02 years
Range	4–14 years
Gender
Male	32 (64%)
Female	18 (36%)
BMI
Mean	18.22 kg/m2
Range	15.4–30.6 kg/m2

Nasal obstruction and resultant mouth breathing were the most common symptoms of UAO exhibited by all (100%) the patients in the study as assessed by the Paediatrics sleep questionnaire. Polysomnography and oximetry were not performed. Remaining symptoms in order of majority were snoring (44%), recurrent sore throat (36%), adenoid facies (30%) and choking spells at night (18%).

28 children (56%) showed grade 4 adenoid hypertrophy and 22 children (44%) showed grade 3 adenoid hypertrophy on diagnostic nasal endoscopy. On oropharyngeal examination, 19 patients (38%) had Brodsky’s grade 4 and 31 patients (62%) had Brodsky’s grade 3 tonsillar enlargement.

80% (40 children) of study members had UAO symptoms due to ATH for a shorter duration of 24 months only. Rest 10 children (20%) had these symptoms for more than 24 months. A significant association was seen between chronicity of symptoms and raised pulmonary artery pressures. [Table 2]

Table 2.

Correlation between chronicity of upper airway obstruction (UAO) symptoms due to Adenotonsillar Hypertrophy (Ath) and development of raised mean pulmonary artery Pressure (MPAP) and pulmonary artery systolic pressure (PASP)

	ATH without raised MPAP & PASP		ATH with raised MPAP & PASP
Chronicity of Symptoms	No. of patients	Percentage	No. of patients	Percentage
≤ 24 Months (2 years)	39	100%	1	9.10%
> 24 Months (2 years)	0	0%	10	90.90%
Total	39	100.0%	11	100.0%
P value	< 0.001
Significance	SIGNIFICANT

11 patients (22%) showed deranged MPAP and PASP on doppler echocardiography. Only 2 children out of these 11 had pressure cut-off values high enough to be diagnosed as PAH. These 2 children were having the disease for 5–6 years.

A significant (p < 0.001) [Tables 3 and 4] improvement was noted in pulmonary artery pressure values (MPAP and PSAP returned to normal) after adenotonsillectomy in 3-month post-operative echocardiography. Nasal obstruction, mouth breathing and choking spells at night were completely eliminated in study members after the surgery. [Table 5]

Table 3.

Comparison of pre-operative and post-operative pulmonary arterial pressure (MPAP and PASP) among children of adenotonsillar hypertrophy with raised pulmonary artery parameters

	Mean	S.D	P value (< 0.05 significant)
Pre-operative MPAP (mm Hg)	24.91	± 1.81	< 0.001 (SIGNIFICANT)
Post-operative MPAP (mm Hg)	17.36	± 1.43
Pre-operative PASP (mm Hg)	29.09	± 4.28	< 0.001 (SIGNIFICANT)
Post-operative PASP (mm Hg)	20.45	± 1.97

Table 4.

Comparison of pre-operative and post-operative pulmonary arterial pressure (MPAP AND PASP) among children of adenotonsillar hypertrophy without raised pulmonary artery parameters

	Mean	S.D	P value (< 0.05 significant)
Pre-operative MPAP (mm Hg)	15.64	± 1.29	0.324 (NOT SIGNIFICANT)
Post-operative MPAP (mm Hg)	15.62	± 1.29
Pre-operative PASP (mm Hg)	18.10	± 1.73	0.324 (NOT SIGNIFICANT)
Post-operative PASP (mm Hg)	18.08	± 1.74

Table 5.

Comparison between pre-operative and post-operative symptoms among the patients

Symptom	Before adeno Tonsillectomy (n = 50)	After adeno Tonsillectomy (n = 50)	Significance (< 0.05 significant)
Nasal obstruction	50 (100%)	0 (0%)	Significant ( p value < 0.001)
Mouth breathing	50 (100%)	0 (0%)	Significant ( p value < 0.001)
Snoring	22 (44%)	0 (0%)	Significant ( p value < 0.001)
Choking spells at night	9 (18%)	0 (0%)	Significant ( p value < 0.001)
Apraxia/ Behavioural Disturbances	18 (36%)	5 (10%)	Significant ( p value < 0.05)
Daytime Sleepiness	20 (40%)	0 (0%)	Significant ( p value < 0.001)
Morning Headaches	12 (24%)	0 (0%)	Significant ( p value < 0.001)
Nocturnal Enuresis	4 (8%)	2 (4%)	Not Significant
Obesity	3 (6%)	3 (6%)	Not Significant

Discussion

ATH is invariably the most common cause of nasopharyngeal and oropharyngeal obstruction in children leading to mouth breathing syndrome (MBS) and OSA. Such diseases, by affecting the upper airways, can cause chronic alveolar hypoventilation, pulmonary vasoconstriction and pulmonary hypertension, which in some cases, are irreversible finally leading on to cor pulmonale. Hence, care of an ATH patient should focus primarily on removing UAO symptoms and the progression of any cardiopulmonary risks which might not be well established in such a patient. Keeping this vision in mind, we hoped for influencing clinical practice through a new approach proposal for patients of MBS. Hence, this study was conducted to look for any preclinical cardiovascular changes to establish association between mouth breathing and raised pulmonary artery pressures in children with ATH and evaluate the reversal of these pressures after adenotonsillectomy.

Duration of Symptoms and Correlation with Impact on Cardiovascular System

The present study findings throw light on the integral role of disease longevity in the pathogenesis of cardiovascular changes. Sustained pulmonary artery vasoconstriction leads to increased PASP and increased MPAP. Logically, it seems that the longer this vasoconstriction is sustained the more effect it would have on PASP and MPAP. This is evident from the fact that 10 out of 50 children of ATH had obstructive symptoms for over 2 years and these same children were found to have altered pulmonary artery parameters when measured by doppler echocardiography. The correlation between duration of disease and raised pulmonary artery pressure was found to be statistically significant. In fact, two children who had developed pulmonary artery hypertension had the longest duration of symptoms, i.e., 5 and 6 years. On the other hand, remaining 40 children who were not suffering from the obstructive symptoms for such a long time were found to be less susceptible to have deranged vascular changes in heart as corroborated by their normal parameters in echocardiography.

Most of the other studies like Lima M S et al. [10], V F Martha et al. [11], Ramos et al. [12] and Tatlipinar et al. [13] did not take into consideration the duration for which their study participants had obstructive symptoms before development of CVS effects thereby limiting our insight into the role of duration of symptoms. Due to unavailability of sufficient data, the effect of duration of UAO on development of PAH in paediatric population needs to be further explored as knowledge of this will help us to make early intervention in the form of adenotonsillectomy and prevent or reverse the vascular damage.

Impact of Longstanding Upper Airway Obstruction on Pulmonary Artery Pressures (MPAP and PASP) Before Adenotonsillectomy

In our study, among 50 participants who underwent doppler echocardiography 1 week prior to adenotonsillectomy, it was observed that 11 children had increased PASP and MPAP. Out of these, 2 children had developed increased pressure in the range of PAH. So, we can safely interpret from these findings that 11 children (22% result prevalence in our study) were affected from persistent UAO in the form of serious CVS complications which could lead to long term consequences like cor pulmonale in future. There are other studies that are in accordance with our study.

In a study by Ismail et al. [14], it was shown that 8 (26.7%) out of their total 30 study children of ATH indicated for adenotonsillectomy, when underwent doppler echocardiography 1 week prior to surgery, had PAH and all of their study subjects had increased PASP. In a study conducted by V M Ramos et al. [12], 30 mouth breathing children due to ATH who had to undergo adenotonsillectomy and 29 nasal breathers were included in study. Both the group members when underwent echocardiography, 7 (23.3%) out of 30 mouth breathing children had increased PASP. Similar results were obtained in studies by V F Martha et al. [10], Tatlipinar et al. [13] and Farriera Nader CMF et al. [15].

However, a study done by Yilmaz et al. [16] with 52 children diagnosed with UAO secondary to ATH showed PH in 27 children (52%) preoperatively. The criteria taken for PH in their study was MPAP > 20 mmHg, which was a much lower value than other studies and our study. Similarly, a high prevalence of PH was seen in another study by Naiboglu et al. [17] with PH prevalence of 84.6%. These two studies are in discordance with our study as the incidence of PH was high compared to our study. This was explained by the fact that a higher MPAP value of > 25 mmHg was taken as the cut-off for classifying children as hypertensive in all other studies described above, including our study as well.

Reversal of Deranged Pulmonary Artery Pressure Values (MPAP and PASP) After Adenotonsillectomy

When MPAP and PASP were compared preoperatively (1 week before adenotonsillectomy) and postoperatively (3 months after adenotonsillectomy) in 11 patients who showed considerable evidence of UAO due to ATH, it was found that average of MPAP before surgery was 24.9 ± 1.81 mm Hg and after surgery was 17.36 ± 1.43 mm Hg. This difference was found to be highly significant (p value < 0.001). The mean of PASP in same 11 case subjects preoperatively and postoperatively was 29.09 ± 4.28 mmHg and 20.45 mm ± 1.97 Hg respectively. This decrease in pressure was also found to be highly statistically significant (p value < 0.001). These statistical analyses corroborate our finding that adenotonsillectomy was successful in reversal of deranged pulmonary artery parameters and prevention of pulmonary artery hypertension or cor pulmonale.

Our findings were further substantiated by the fact that mean of PASP and MPAP preoperatively and postoperatively in 39 children who did not have any CVS effects in the form of raised pulmonary artery pressure due to ATH came out to be non-significant (p value = 0.324). Ismail et al. [14] also showed highly statistically significant decrease in the PASP, the mean value of preoperative PASP was (34.21 +/-6.7), 4 months postoperative PASP was (16.21 ± 7.59), p value < 0.001. V F Martha et al. [11] study gave results similar to our study. PAH was verified in 12 (36%) of the 33 patients with ATH. Adenoidectomy or adenotonsillectomy was associated to a significant 27% decrease in mean PAP (27 ± 2.8 to 20 ± 5.1 mmHg, p < 0.001) and to a non-significant 26% decrease in systolic PAP (35 ± 6.2 mmHg to 25 ± 0.5 mmHg, p value- 0.243).

A study by V M Ramos et al. [12] and Sameema et al. [18] also stated supportive findings.

Such reversal of pulmonary artery pressure after adenotonsillectomy can be attributed to the removal of UAO and state of hypoxia in body after surgery, both of which were found to be the main driving force for the development of cardiovascular sequelae. Not only there was retraction of vascular damage, other symptoms like choking spells at night, apraxia, snoring, nasal obstruction, and even behavioral disturbances were reduced in children postoperatively on follow up visits as assessed by the paediatric sleep questionnaire. However, duration of which varied in different cases. Some children were relieved of their symptoms 6 weeks postoperatively while others took 3 months.

Conclusion

The current study suggests that children with chronic ATH, especially with grade 3 and 4 hypertrophy, are at considerable risk for cardiopulmonary sequelae since we saw that 11 patients (22%) showed deranged pulmonary artery pressures and two of these had pulmonary artery hypertension on doppler echocardiography. Thus, PAH and cor pulmonale must always be considered in the mind of an otorhinolaryngology surgeon during management of ATH. This is necessary because even before clinical signs of PAH occur, it can be screened during preoperative workup of chronic ATH patients. The sooner we catch the disease, the more its progression to heart failure can be prevented as a highly significant (p < 0.001) improvement was noted in pulmonary artery pressure values which returned to normal after adenotonsillectomy in 3-month postoperative echocardiography. Therefore, doppler echocardiography can be a powerful tool in identifying development of cardiovascular complications and helping the surgeon in decision making for timely adenotonsillectomy.

Limitations

A small study population was taken. A larger population is required to validate the results with more strength. Also, a control group was not taken which would have helped establish the result with greater affirmation. Moreover, no objective tests were done to diagnose OSA like polysomnography and oximetry.

Funding

No funding was received for the conduction of the study at any stage.

Declarations

The authors did not receive support from any organization for the submitted work.

The authors have no competing interests to declare that are relevant to the context of this article.

The authors have no relevant financial or non-financial interests to disclose.

Ethical statement

The study protocol was approved by the Institutional Review Board for Ethical Clearance of Government Medical College and Rajindra Hospital and it was performed in accordance with the Code of Ethics of the World Medical Association according to the Declaration of Helsinki of 1975, as revised in 2000. Informed consent has been taken from the patients for publication.