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The impact of adenotonsillectomy on pulmonary arterial pressure in West African children with adenotonsillar hypertrophy
International Journal of Pediatric Otorhinolaryngology 92 (2017) 151e155
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: http://www.ijporlonline.com/
The impact of adenotonsillectomy on pulmonary arterial pressure in West African children with adenotonsillar hypertrophy Foster T. Orji a, *, Fortune A. Ujunwa b, Nnaemeka G. Umedum c, Onyinyechi Ukaegbe a a
Department of Otolaryngology, University of Nigeria Enugu Campus, Nigeria Department of Pediatric Cardiology, University of Nigeria Teaching Hospital Enugu, Nigeria c Department of Otolaryngology, University of Nigeria Teaching Hospital Enugu, Nigeria b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 September 2016 Received in revised form 19 November 2016 Accepted 23 November 2016 Available online 25 November 2016
Objectives: To assess the improvement or otherwise, in the mean pulmonary arterial pressure (mPAP) among children with adenotonsillar hypertrophy (ATH) after adenotonsillectomy (AT), and to examine the impact of timing of surgery as well as the patients' characteristics on the mPAP changes. Methods: We included 39 children with ATH in this study. The adenoidal enlargement was evaluated radiologically with adenoid nasopharyngeal ratio (ANR) parameter from lateral neck radiograph, whereas the clinical assessment of adeno-tonsillar obstruction was conducted with the ‘symptom score’. Pulmonary arterial pressure (PAP) measurement was performed noninvasively by Doppler echocardiography. All patients underwent adenotonsillectomy (AT). After 6 weeks, they were subjected again to clinical and echocardiographic assessments, and the mean pulmonary arterial pressures (mPAP) were then compared. The mPAP changes after AT were further related to the grades of ANR, symptom scores, tonsillar size, and timing of AT. Results: The preoperative mPAP was 23.46 mmHg and was 18.98 mmHg post-operatively (P ¼ 0.003). Seventeen of subjects (43.6%) had pulmonary hypertension (PH) (mPAP 25 mmHg) preoperatively, out of which 14 (82%) decreased to normal range 6 weeks after AT. Non-reversal of pulmonary hypertension was associated with ANR > 0.75 (P ¼ 0.043), but was not related to the timing of surgery, tonsillar size, and symptom score. Significant reduction in mPAP was more likely with ANR 0.75 and pre-operative mPAP 25 mmHg. All the symptoms also improved significantly after AT. Conclusion: Elevated PAP due to ATH in children was mostly reversible by AT irrespective of the timing of surgery, symptom severity, and tonsillar size, but gross enlargement of adenoids seem to be associated with non-reversal of PH. © 2016 Elsevier Ireland Ltd. All rights reserved.
Keywords: Adenotonsillar hypertrophy Pulmonary arterial pressure Adenotonsillectomy Children Echocardiography
1. Introduction Adenoid hypertrophy or adenotonsillar hypertrophy (ATH) remains the most common cause of upper airway obstruction and obstructive sleep apnoea (OSA) in children. Untreated ATH in some cases have resulted in wide range of cardiopulmonary changes including: pulmonary hypertension (PH) and cor pulmonale, cardiac failure, and systemic hypertension. Incidentally, most of the reported cases of severe cardiopulmonary complications are relatively rare and have been documented to resolve after adenoidectomy or adenotonsillectomy (AT) [1e4]. More recent reports have shown that majority of the affected children seem to belong to a
* Corresponding author. Department of Otolaryngology, University of Nigeria Teaching Hospital Enugu, Nigeria. E-mail address: [email protected] (F.T. Orji). http://dx.doi.org/10.1016/j.ijporl.2016.11.023 0165-5876/© 2016 Elsevier Ireland Ltd. All rights reserved.
larger group that suffer partial upper airway obstruction on account of ATH, with asymptomatic milder cardiopulmonary changes [5,6]. These children who have milder cardiopulmonary sequel from obstructive ATH have not been investigated in details. These cardiopulmonary changes can be monitored effectively with doppler echocardiography [7]. The upper airway obstructive symptoms of ATH in general, including the sleep disordered breathing, have been shown to be effectively treated with AT [8,9]. However, the questions of whether milder forms of sleep disorder breathing in children are associated with cardiovascular changes and, what factors influence the reversal of cor-pulmonale after AT are yet to be examined in details. This present study was designed to examine the improvements or otherwise, of the mean pulmonary arterial pressure (mPAP) after adenotonsillectomy in children with ATH, and to examine the impact of timing of surgery as well as the clinical and radiological characteristics of patients on the mPAP changes.
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2. Method The study population consist of 39 consecutively recruited children (23 (59%) boys and 16 girls (41%) who underwent adenotonsillectomy (AT) or adenoidectomy on account of upper airway obstruction from ATH, in Otolaryngology department of the University of Nigeria Teaching Hospital Enugu during 32 months period ending February 2016. 2.1. Ethical consideration Approval for the study was given by the institution ethical review committee. Written informed consent was obtained from the parents or care givers of each of the children included in the study. 2.2. Recruitment of participants Subjects included in the study were children with a clinical diagnosis of adenoid hypertrophy (AH) with or without tonsillar hypertrophy as the only cause of upper airway obstruction, those who completed the follow up schedule, and those that gave consent for the study. Participants excluded had previous adenoidectomy/adenotonsillectomy (AT), or had other causes of upper airway obstruction (such as: nasal septal deviation, craniofacial abnormalities), or other cases of sleep apnoea (such as obesity or cerebral palsy). Participants were also excluded if they had co-morbidities that would otherwise explain PH (such as previous history of cardiac disease, or discovered during echocardiography, HIV infection, chronic obstructive lung disease, and sickle cell anaemia). The following procedure was adopted for all the participants. 2.3. Pre- and post-operative assessment At the point of first contact, history was obtained from the caregivers and physical examination performed on all the children including a general, ENT and cardiovascular assessment. Assessment of the severity of the upper airway obstruction was carried out by grading the following symptoms: snoring, daytime stertor, mouth breathing during sleep, daytime mouth breathing, daytime hypersomnolence, obstructive breathing during sleep, nasal obstruction. The symptoms were graded with the following responses: ‘absent’, ‘occasionally’ (mild grade), and ‘always’ (severe grade). The responses of ‘occasionally’ and ‘always’ attracted scores of ‘1’ and ‘2’ respectively, whereas ‘absent’ answer was scored ‘0’. There was a maximum of 14 points. The overall symptom score was classified as either ‘mild’ (1e5 points), moderate (6e10 points), or severe (>10 points). No participant in this study had symptom score less than 6-points. The resolution/improvement or otherwise, of sleep disturbances and breathing difficulties after AT, was assessed by comparing the pre- and post-operative mean symptom scores. The size of the tonsils was graded during oropharyngeal examination on a scale of 1e4 employing the Brodsky classification as previously described [7,10]: Grade 1 tonsils represented tonsils confined to the faucial pillars; grade 2 was tonsils that extended just outside the pillars; grade 3 - tonsils extending outside the pillars but not meeting in the midline; grade 4 e were tonsils meeting in the midline. All the patients in this study had a minimum of grade 2 tonsils. Radiologic examination: included lateral plain x-ray of the nasopharynx. The size of the adenoid was assessed with the ‘adenoid nasopharyngeal ratio’ (ANR) parameter as previously described [11]. The adenoid hypertrophy was considered mild if AN ratio was 0.62, moderate ¼ 0.63e0.75, gross ¼ >0.75. All the
children in this study had an ANR 0.63. Following routine cardiovascular examination, their cardiac functions were all evaluated pre-operatively using twodimensional Coloured Doppler ‘SONOSCAPE SSI-5000’ Echocardiography, with 3.5 Hz transducer. It was equipped with the capability for M-mode, two-dimensional, 3-dimensional, pulsed wave, continuous wave and colour flow Doppler echocardiographic measurements. The mean pulmonary artery systolic pressure (mPAP) was determined by using the continuous wave Doppler to get the peak tricuspid regurgitation jet velocity and the pressure gradient. This was substituted in the Bernoulli Equation: PASP ¼ RVSP ¼ 4 (VTR)2 þ RAP. Pulmonary hypertension (PH) was defined by mPAP 25 mmHg. The raised PAP was regarded as borderline for mPAP 20 25 mmHg, and normal PAP (mPAP <20 mmHg). All the children were subjected to similar echocardiographic examination at 6 weeks postoperatively. The obtained changes in mPAP post-operatively were compared with the tonsil grades, ANR and the overall symptom scores as well as the timing of AT (defined in relation to the Onset of symptoms/ duration). 2.4. Operative procedure - Adenoidectomy was carried out for all patients using conventional curettage technique. Tonsillectomy was by conventional dissection technique. Anaesthetic induction was done using isoflorane or halothane in oxygen to prevent sudden carbon dioxide wash and apnea.
2.5. Statistical analysis The ‘Statistical Package for Social Sciences’ (SPSS) version 16.5 for Windows, was utilised in the analysis. The preoperative and postoperative echocardiographic parameters were compared with paired sample t-test, and the mPAP changes were compared among participants of different clinical and radiologic parameters with Fisher's exact test. Statistical significance was set at P < 0.05. 3. Results Sixty one children who underwent adenoidectomy/AT were evaluated but 39 completed the follow up schedule and therefore met our inclusion criteria. All the children underwent adenotonsillectomy. Their mean was 4.6 years with a median of 3.4years and 25e75 percentile range of 2.4e5.8 years. Table 1 shows the age distribution of the patients in relation to their mPAP. The mPAP was recorded highest among the 9 youngest participants aged <2 years, but the differences in the mPAP among the age groups were not significant (P ¼ 0.847). In the pre-operative period, PH (mPAP 25 mmHg) was observed in a total of 17 children which was distributed in 56%, 35%, and 46% of the age groups <2 years, 2e5 years, and >5 years respectively. In the post-operative periods, the mPAP of 14 of the children normalised below 25 mmHg, whereas it remained above 25 mmHg in 3 of children, giving 82.4% resolution of pulmonary hypertension following AT (P ¼ 0.000). Table 2 showed the mPAP before, and 6 weeks after AT. There was significant decrease in mPAP postoperatively (paired sample ttest, P ¼ 0.003). The decrease in mPAP following AT/adenoidectomy was most remarkable among the children with pre-operative pulmonary hypertension with an average of 6.8 mmHg drop in mPAP (P ¼ 0.007). The recorded changes in the mPAP following adenoidectomy/AT among different pre-operative parameters were outlined in Tables 3 and 4. The reduction in the mPAP following surgery was
F.T. Orji et al. / International Journal of Pediatric Otorhinolaryngology 92 (2017) 151e155
153
Table 1 The age distribution of 39 children with adenotonsillar hypertrophy (ATH) in relation with the mean pulmonary arterial pressures (mPAP). Age groups
No of patients
No with PH (25 mmHg)
mPAP(mmHg) ± SD
P value
<2 years 2e5 years >5 years
9 17 13
5 6 6
24.60 ± 7.51 23.05 ± 5.30 23.21 ± 7.92
*0.847
SD ¼ standard deviation; PH ¼ pulmonary hypertension; *ANOVA test.
Table 2 Comparison of preoperative mPAP of 39 children with ATH with the postoperative values.
Pre-operative Value Post-Operative Value
mPAP (SD)
Statistics Range
*95% CI
Paired t-test
P value
23.46 (6.6) 18.98 (5.2)
11.6e39.3 8.9e28.6
2.58e6.38
4.77
0.003
SD ¼ standard deviation; *95% Confidence interval.
expressed as a percentage of the pre-operative value. It was graded as moderate (<25% decrease) and significant (25% decrease). It ranged from 3% to 69% reduction. However, 2 (5%) of the children recorded increases in their post-operative mPAP, (12% and 19% increase respectively). Both children belonged to the group of children that had normal pre-operative mPAP. Overall, 12 children had more than 25% decrease of their mPAP, with majority recording only a moderate reduction. Significant proportions of the group of children with pre-operative ANR measurements of >0.75 (gross obstruction) and those with pre-operative mPAP exceeding 25 mmHg (pulmonary hypertension) recorded a significant decrease in their mPAP (P ¼ 0.033 and 0.021 respectively). The changes in the post-operative mPAP did not differ significantly in respect of the overall symptom score groups, tonsillar sizes as well as symptom duration/timing of surgery. The change in symptom scores were calculated by subtracting the postoperative mean scores (total and individual symptoms) from the corresponding preoperative values. The symptom scores in the pre- and post-operative periods were compared in Table 5. All the symptoms improved significantly after surgery with the highest improvement occurring in the symptom domains of obstructive breathing during sleep, snoring, and daytime stertor respectively. Regarding the overall symptom score, it recorded a very significant changed in the post operative periods (P ¼ 0.000). However, insignificant changes in the symptom scores were observed in two children who were also among the children with unresolved PH. They continued to snore and mouth breath most nights and even at daytime after AT. Repeat radiographs of the
Table 3 Non-reversal of *PH in relation to duration of symptoms, symptom score and adenoid-nasopharyngeal ratio among 17 participants with pre-operative PH. Post-operative mPAP Persistent PH
Resolved PH
Timing of adenotonsillectomy (in relation to onset of symptoms) <12 months 1 6 12 months 2 8 Overall symptom score 6-10 points 2 3 >10 points 1 11 Adenoid nasopharyngeal ratio 0.75 0 9 >0.75 3 5 Tonsillar size (Brodsky grade) grades 1 & 2 0 3 grades 3 & 4 3 11 *PH: pulmonary hypertension, ** Fisher's exact test; *** Significant.
P value**
0.781
0.119
0.043***
0.377
nasopharynx confirmed significantly improved airway despite the persistent symptoms. They were further followed up and significant improvements were recorded at 3 months.
4. Discussion Cor pulmonale and congestive heart failure are recognised as potential sequels of untreated obstructive sleep apnoea syndrome (OSAS) resulting from ATH in children [1,3,12]. Adenotonsillectomy has also been widely accepted as the treatment of choice for cardiovascular abnormalities resulting from ATH [4e6,12]. In the 1950s, childhood OSAS was diagnosed mainly by cardiologists and endocrinologists when children presented in heart failure or severe growth impairment [5]. But currently, in the wake of increase awareness and higher frequency of AT for OSAS, majority of patients with ATH present with very mild symptoms or none, that relate to the cardiopulmonary system. However symptomless chronic cardiopulmonary changes may slowly occur in these children [6,12]. The more relevant questions are: whether milder forms of sleep disorder breathing in children are associated with cardiovascular changes, what factors influence the reversal of corpulmonale after AT, whether development of permanent pulmonary hypertension is dependent on the duration of upper airway obstruction before instituting AT treatment. In this present study, 39 cases were eligible for statistical analysis, out of which 43.6% had pulmonary hypertension. Incidentally we studied children whose cardiovascular changes were mild and not serious yet, and have not shown obvious abnormalities detectable on chest x-rays of our patients. All the PH in this study were mild with mPAP < 41 mmHg [13]. In the absence of detectable abnormalities on chest x-rays, early detection of cardiovascular abnormalities were easily done by monitoring mPAPs of our children with Doppler echocardiography. Most previous similar studies also reported studying children with mild cardiovascular changes in their series with mPAP of <40 mmHg [4e6,12,14]. In one study [15], it was reported that the mild form of cor pulmonale due to adenotonsillar enlargement could not be diagnosed clinically. In another study, Tal et al. [16] concluded that the right ventricular function may be compromised in children with obstructive sleep apnea even before the clinical signs of cardiac involvement are being detectable. Our study showed a significant reduction of mPAP postoperatively, with complete reversal of PH in more than 82% of the index cases. Similar results have been reported by other researchers. In one study [6], 51.9% of the eligible cases were reported to have PH although pulmonary hypertension was defined with
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Table 4 The extent of post-operative mPAP changes in relation to pre-operative measurements. Pre-operative parameters
Post-operative mPAP changes
P value
25% reduction Overall symptom score 7e10 points 5 >10 points 7 Adenoid nasopharyngeal ratio 0.75 8 >0.75 4 Tonsillar size (Brodsky grade) grades 1 & 2 2 grades 3 & 4 10 Pulmonary arterial pressure <25 mmHg 3 25 mmHg 9 Timing of adenotonsillectomy (in relation to onset of symptoms) <12 months 5 12 months 7
<25% reduction
Increased
4 21
1 1
*0.178
9 16
0 2
*0.033
5 20
1 1
* 0.554
17 8
2 0
*0.021
10 15
0 2
*0.743
*Fisher's exact test.
Table 5 Comparison of pre- and post-operative mean symptom scores n ¼ 39. Symptom domains
Pre-surgery mean score
Post-surgery mean score
Change score* (95% CI)
zP value
Overall symptom score Snoring Nocturnal mouth breathing Obstructive breathing during sleep Nasal obstruction Daytime stertor Daytime mouth breathing Daytime Hypersomnolence
8.5 1.7 1.4 1.6 1.4 1.3 1.1 1.2
3.1 0.5 1.0 0.2 0.9 0.2 0.7 0.8
5.4 1.2 0.4 1.4 0.5 1.1 0.4 0.3
0.000 0.000 0.021 0.000 0.012 0.000 0.001 0.037
(4.7e6.1) (0.9e1.4) (0.1e0.6) (1.2e1.6) (0.1e0.7) (0.9e1.4) (0.2e0.7) (0.2e0.6)
CI ¼ 95% Confidence interval, * ¼ pre-surgery mean minus post-surgery mean; z ¼ Paired sample t-test.
mPAP of 20 mmHg in contrast to our study where PH was defined by mPAP 25 mmHg. However, 67% of children with PH in the aforementioned study had normal mPAP values after AT, while the remaining 9 children were reported to have lower mPAP values compared with preoperative ones [6]. Abdel-Aziz [5] reported significant improvement of pre-operative cardiovascular parameters including mPAP. However the proportion of the cases with PH was not stated. Moreover there was relatively limited number of participants (18 children) in their study. Miman et al. [12] documented complete resolution of pre-operative echocardiographic pathologies, including normalization of mPAP in all the 18 patients with PH secondary to ATH, 3 month following AT. In contrast not all the children with PH in our study had complete reversal of their PH. As illustrated in Table 3, PH persisted in 3 of the participants at 6 week post-operative echocardiographic re-assessments. Although the number of unresolved PH seems too small for any conclusive statistical significance to be derived, non-resolution of PH seems to potentially correlated with gross adenoidal hypertrophy, as all of them were among the group of children who had ANR > 0.75 (P ¼ 0.043). However it was possible that our relatively shorter post-operative re-evaluation period of 6 weeks, (which was adopted in our study to minimise the potential loss of participants to follow up because of our socio-cultural peculiarities), might have accounted for the apparent non-resolution of PH. One may also speculate that suboptimal compliance or viral URT infections of these children during 2D echo measurement of mPAP, as well as incomplete resection of adenoid tissue or rapid re-growth/ enlargement of adenoid tissue may have played roles in these children. In a systematic review of the effects of AT on cardiovascular parameters in children with obstructive sleep apnoea Dawn et al.
[4] reported that out of the analysed 14 articles, 6 reported improvement in mean pulmonary artery pressures, 7 reported improvement in echocardiographic findings in general, after AT for OSAS. However they made the following observations: that there was none uniformity in the defining criteria for PH thereby making comparison difficult, and that none of the studies examined the correlation between the various cardiovascular parameters and OSAS severity. In this present study we attempted to evaluate whether the improvements recorded in the post-operative mPAP were related to symptom severity (symptom score), severity of adenoidal airway obstruction (adenoid-nasopharyngeal ratio), size of obstructive tonsils, duration of obstructive symptoms and the pre-operative mPAP values. We observed that significant reduction of mPAP (>25%) was significantly less likely to be encountered in children with gross adenoidal hypertrophy, but was more likely in those with pre-operative mPAP exceeding 25 mmHg. In other words, children with PH were more likely to have significant reductions of their pulmonary arterial pressure following AT than children with normal mPAP. However, the reduction of mPAP occurred after AT irrespective of the degree of pre-operative symptom severity, or duration of the symptoms before AT. The improvement did not also correlate with the size of the tonsils. Oran et al. [21] reported significant reversal of pulmonary hypertension among 20 children with different URT obstructions compared to 20 healthy controls after AT which supports our findings that PH is readily amenable to AT. However, similar to our data, Naigoblu et al. [22] reported that these observed significant reversal of PH occur regardless of the symptom severity. Our major limitation was our inability to perform a polysomnography which is the gold standard for diagnosis of OSA.
F.T. Orji et al. / International Journal of Pediatric Otorhinolaryngology 92 (2017) 151e155
However polysomnographic evaluation is not a routine clinical investigation. It is cumbersome to apply and is further compounded by its limited availability and additional cost. Unlike polysomnograghy that measures derangements in physiologic parameters during sleep; clinical evaluation focuses on the physical problems and functional limitations consequent on upper airway obstruction as reported by caregivers. However, predictive accuracy of clinically suspected OSAS may be as low as 30% when polysomnograghy testing was performed as well [17,18]. Nevertheless, standardised symptom grading has been shown to reliably evaluate the degree of upper airway obstruction by ATH in children [19,20]. In this present study the overall symptom score and the scores for all individual symptoms showed significant dramatic improvement after AT, which seem to correlate with the improvement in the mPAP. Moreover, the two children that showed no significant improvement in their symptoms also correspondingly showed persistence of their PH after AT. Our study was also limited by the relative low number of participants as well as the relative shorter follow-up period of 6 weeks which seems to be an early time point to figure out the exact resolution of pulmonary hypertension. In conclusion, PH due to ATH may be reversible by adenotonsillectomy. The reversal seems not related to the timing of the surgery or to the symptom severity, but the degree of mPAP improvement may be related to the radiological size of adenoid and the pre-operative mPAP. Cardiopulmonary status of children with ATH can readily be assessed by echocardiographic examinations and may be beneficial in taking useful decision before adenotonsilectomy and for assessing the benefit of surgery after AT. Conflict of interest None declared. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: http://www.ijporlonline.com/
The impact of adenotonsillectomy on pulmonary arterial pressure in West African children with adenotonsillar hypertrophy Foster T. Orji a, *, Fortune A. Ujunwa b, Nnaemeka G. Umedum c, Onyinyechi Ukaegbe a a
Department of Otolaryngology, University of Nigeria Enugu Campus, Nigeria Department of Pediatric Cardiology, University of Nigeria Teaching Hospital Enugu, Nigeria c Department of Otolaryngology, University of Nigeria Teaching Hospital Enugu, Nigeria b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 September 2016 Received in revised form 19 November 2016 Accepted 23 November 2016 Available online 25 November 2016
Objectives: To assess the improvement or otherwise, in the mean pulmonary arterial pressure (mPAP) among children with adenotonsillar hypertrophy (ATH) after adenotonsillectomy (AT), and to examine the impact of timing of surgery as well as the patients' characteristics on the mPAP changes. Methods: We included 39 children with ATH in this study. The adenoidal enlargement was evaluated radiologically with adenoid nasopharyngeal ratio (ANR) parameter from lateral neck radiograph, whereas the clinical assessment of adeno-tonsillar obstruction was conducted with the ‘symptom score’. Pulmonary arterial pressure (PAP) measurement was performed noninvasively by Doppler echocardiography. All patients underwent adenotonsillectomy (AT). After 6 weeks, they were subjected again to clinical and echocardiographic assessments, and the mean pulmonary arterial pressures (mPAP) were then compared. The mPAP changes after AT were further related to the grades of ANR, symptom scores, tonsillar size, and timing of AT. Results: The preoperative mPAP was 23.46 mmHg and was 18.98 mmHg post-operatively (P ¼ 0.003). Seventeen of subjects (43.6%) had pulmonary hypertension (PH) (mPAP 25 mmHg) preoperatively, out of which 14 (82%) decreased to normal range 6 weeks after AT. Non-reversal of pulmonary hypertension was associated with ANR > 0.75 (P ¼ 0.043), but was not related to the timing of surgery, tonsillar size, and symptom score. Significant reduction in mPAP was more likely with ANR 0.75 and pre-operative mPAP 25 mmHg. All the symptoms also improved significantly after AT. Conclusion: Elevated PAP due to ATH in children was mostly reversible by AT irrespective of the timing of surgery, symptom severity, and tonsillar size, but gross enlargement of adenoids seem to be associated with non-reversal of PH. © 2016 Elsevier Ireland Ltd. All rights reserved.
Keywords: Adenotonsillar hypertrophy Pulmonary arterial pressure Adenotonsillectomy Children Echocardiography
1. Introduction Adenoid hypertrophy or adenotonsillar hypertrophy (ATH) remains the most common cause of upper airway obstruction and obstructive sleep apnoea (OSA) in children. Untreated ATH in some cases have resulted in wide range of cardiopulmonary changes including: pulmonary hypertension (PH) and cor pulmonale, cardiac failure, and systemic hypertension. Incidentally, most of the reported cases of severe cardiopulmonary complications are relatively rare and have been documented to resolve after adenoidectomy or adenotonsillectomy (AT) [1e4]. More recent reports have shown that majority of the affected children seem to belong to a
* Corresponding author. Department of Otolaryngology, University of Nigeria Teaching Hospital Enugu, Nigeria. E-mail address: [email protected] (F.T. Orji). http://dx.doi.org/10.1016/j.ijporl.2016.11.023 0165-5876/© 2016 Elsevier Ireland Ltd. All rights reserved.
larger group that suffer partial upper airway obstruction on account of ATH, with asymptomatic milder cardiopulmonary changes [5,6]. These children who have milder cardiopulmonary sequel from obstructive ATH have not been investigated in details. These cardiopulmonary changes can be monitored effectively with doppler echocardiography [7]. The upper airway obstructive symptoms of ATH in general, including the sleep disordered breathing, have been shown to be effectively treated with AT [8,9]. However, the questions of whether milder forms of sleep disorder breathing in children are associated with cardiovascular changes and, what factors influence the reversal of cor-pulmonale after AT are yet to be examined in details. This present study was designed to examine the improvements or otherwise, of the mean pulmonary arterial pressure (mPAP) after adenotonsillectomy in children with ATH, and to examine the impact of timing of surgery as well as the clinical and radiological characteristics of patients on the mPAP changes.
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2. Method The study population consist of 39 consecutively recruited children (23 (59%) boys and 16 girls (41%) who underwent adenotonsillectomy (AT) or adenoidectomy on account of upper airway obstruction from ATH, in Otolaryngology department of the University of Nigeria Teaching Hospital Enugu during 32 months period ending February 2016. 2.1. Ethical consideration Approval for the study was given by the institution ethical review committee. Written informed consent was obtained from the parents or care givers of each of the children included in the study. 2.2. Recruitment of participants Subjects included in the study were children with a clinical diagnosis of adenoid hypertrophy (AH) with or without tonsillar hypertrophy as the only cause of upper airway obstruction, those who completed the follow up schedule, and those that gave consent for the study. Participants excluded had previous adenoidectomy/adenotonsillectomy (AT), or had other causes of upper airway obstruction (such as: nasal septal deviation, craniofacial abnormalities), or other cases of sleep apnoea (such as obesity or cerebral palsy). Participants were also excluded if they had co-morbidities that would otherwise explain PH (such as previous history of cardiac disease, or discovered during echocardiography, HIV infection, chronic obstructive lung disease, and sickle cell anaemia). The following procedure was adopted for all the participants. 2.3. Pre- and post-operative assessment At the point of first contact, history was obtained from the caregivers and physical examination performed on all the children including a general, ENT and cardiovascular assessment. Assessment of the severity of the upper airway obstruction was carried out by grading the following symptoms: snoring, daytime stertor, mouth breathing during sleep, daytime mouth breathing, daytime hypersomnolence, obstructive breathing during sleep, nasal obstruction. The symptoms were graded with the following responses: ‘absent’, ‘occasionally’ (mild grade), and ‘always’ (severe grade). The responses of ‘occasionally’ and ‘always’ attracted scores of ‘1’ and ‘2’ respectively, whereas ‘absent’ answer was scored ‘0’. There was a maximum of 14 points. The overall symptom score was classified as either ‘mild’ (1e5 points), moderate (6e10 points), or severe (>10 points). No participant in this study had symptom score less than 6-points. The resolution/improvement or otherwise, of sleep disturbances and breathing difficulties after AT, was assessed by comparing the pre- and post-operative mean symptom scores. The size of the tonsils was graded during oropharyngeal examination on a scale of 1e4 employing the Brodsky classification as previously described [7,10]: Grade 1 tonsils represented tonsils confined to the faucial pillars; grade 2 was tonsils that extended just outside the pillars; grade 3 - tonsils extending outside the pillars but not meeting in the midline; grade 4 e were tonsils meeting in the midline. All the patients in this study had a minimum of grade 2 tonsils. Radiologic examination: included lateral plain x-ray of the nasopharynx. The size of the adenoid was assessed with the ‘adenoid nasopharyngeal ratio’ (ANR) parameter as previously described [11]. The adenoid hypertrophy was considered mild if AN ratio was 0.62, moderate ¼ 0.63e0.75, gross ¼ >0.75. All the
children in this study had an ANR 0.63. Following routine cardiovascular examination, their cardiac functions were all evaluated pre-operatively using twodimensional Coloured Doppler ‘SONOSCAPE SSI-5000’ Echocardiography, with 3.5 Hz transducer. It was equipped with the capability for M-mode, two-dimensional, 3-dimensional, pulsed wave, continuous wave and colour flow Doppler echocardiographic measurements. The mean pulmonary artery systolic pressure (mPAP) was determined by using the continuous wave Doppler to get the peak tricuspid regurgitation jet velocity and the pressure gradient. This was substituted in the Bernoulli Equation: PASP ¼ RVSP ¼ 4 (VTR)2 þ RAP. Pulmonary hypertension (PH) was defined by mPAP 25 mmHg. The raised PAP was regarded as borderline for mPAP 20 25 mmHg, and normal PAP (mPAP <20 mmHg). All the children were subjected to similar echocardiographic examination at 6 weeks postoperatively. The obtained changes in mPAP post-operatively were compared with the tonsil grades, ANR and the overall symptom scores as well as the timing of AT (defined in relation to the Onset of symptoms/ duration). 2.4. Operative procedure - Adenoidectomy was carried out for all patients using conventional curettage technique. Tonsillectomy was by conventional dissection technique. Anaesthetic induction was done using isoflorane or halothane in oxygen to prevent sudden carbon dioxide wash and apnea.
2.5. Statistical analysis The ‘Statistical Package for Social Sciences’ (SPSS) version 16.5 for Windows, was utilised in the analysis. The preoperative and postoperative echocardiographic parameters were compared with paired sample t-test, and the mPAP changes were compared among participants of different clinical and radiologic parameters with Fisher's exact test. Statistical significance was set at P < 0.05. 3. Results Sixty one children who underwent adenoidectomy/AT were evaluated but 39 completed the follow up schedule and therefore met our inclusion criteria. All the children underwent adenotonsillectomy. Their mean was 4.6 years with a median of 3.4years and 25e75 percentile range of 2.4e5.8 years. Table 1 shows the age distribution of the patients in relation to their mPAP. The mPAP was recorded highest among the 9 youngest participants aged <2 years, but the differences in the mPAP among the age groups were not significant (P ¼ 0.847). In the pre-operative period, PH (mPAP 25 mmHg) was observed in a total of 17 children which was distributed in 56%, 35%, and 46% of the age groups <2 years, 2e5 years, and >5 years respectively. In the post-operative periods, the mPAP of 14 of the children normalised below 25 mmHg, whereas it remained above 25 mmHg in 3 of children, giving 82.4% resolution of pulmonary hypertension following AT (P ¼ 0.000). Table 2 showed the mPAP before, and 6 weeks after AT. There was significant decrease in mPAP postoperatively (paired sample ttest, P ¼ 0.003). The decrease in mPAP following AT/adenoidectomy was most remarkable among the children with pre-operative pulmonary hypertension with an average of 6.8 mmHg drop in mPAP (P ¼ 0.007). The recorded changes in the mPAP following adenoidectomy/AT among different pre-operative parameters were outlined in Tables 3 and 4. The reduction in the mPAP following surgery was
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Table 1 The age distribution of 39 children with adenotonsillar hypertrophy (ATH) in relation with the mean pulmonary arterial pressures (mPAP). Age groups
No of patients
No with PH (25 mmHg)
mPAP(mmHg) ± SD
P value
<2 years 2e5 years >5 years
9 17 13
5 6 6
24.60 ± 7.51 23.05 ± 5.30 23.21 ± 7.92
*0.847
SD ¼ standard deviation; PH ¼ pulmonary hypertension; *ANOVA test.
Table 2 Comparison of preoperative mPAP of 39 children with ATH with the postoperative values.
Pre-operative Value Post-Operative Value
mPAP (SD)
Statistics Range
*95% CI
Paired t-test
P value
23.46 (6.6) 18.98 (5.2)
11.6e39.3 8.9e28.6
2.58e6.38
4.77
0.003
SD ¼ standard deviation; *95% Confidence interval.
expressed as a percentage of the pre-operative value. It was graded as moderate (<25% decrease) and significant (25% decrease). It ranged from 3% to 69% reduction. However, 2 (5%) of the children recorded increases in their post-operative mPAP, (12% and 19% increase respectively). Both children belonged to the group of children that had normal pre-operative mPAP. Overall, 12 children had more than 25% decrease of their mPAP, with majority recording only a moderate reduction. Significant proportions of the group of children with pre-operative ANR measurements of >0.75 (gross obstruction) and those with pre-operative mPAP exceeding 25 mmHg (pulmonary hypertension) recorded a significant decrease in their mPAP (P ¼ 0.033 and 0.021 respectively). The changes in the post-operative mPAP did not differ significantly in respect of the overall symptom score groups, tonsillar sizes as well as symptom duration/timing of surgery. The change in symptom scores were calculated by subtracting the postoperative mean scores (total and individual symptoms) from the corresponding preoperative values. The symptom scores in the pre- and post-operative periods were compared in Table 5. All the symptoms improved significantly after surgery with the highest improvement occurring in the symptom domains of obstructive breathing during sleep, snoring, and daytime stertor respectively. Regarding the overall symptom score, it recorded a very significant changed in the post operative periods (P ¼ 0.000). However, insignificant changes in the symptom scores were observed in two children who were also among the children with unresolved PH. They continued to snore and mouth breath most nights and even at daytime after AT. Repeat radiographs of the
Table 3 Non-reversal of *PH in relation to duration of symptoms, symptom score and adenoid-nasopharyngeal ratio among 17 participants with pre-operative PH. Post-operative mPAP Persistent PH
Resolved PH
Timing of adenotonsillectomy (in relation to onset of symptoms) <12 months 1 6 12 months 2 8 Overall symptom score 6-10 points 2 3 >10 points 1 11 Adenoid nasopharyngeal ratio 0.75 0 9 >0.75 3 5 Tonsillar size (Brodsky grade) grades 1 & 2 0 3 grades 3 & 4 3 11 *PH: pulmonary hypertension, ** Fisher's exact test; *** Significant.
P value**
0.781
0.119
0.043***
0.377
nasopharynx confirmed significantly improved airway despite the persistent symptoms. They were further followed up and significant improvements were recorded at 3 months.
4. Discussion Cor pulmonale and congestive heart failure are recognised as potential sequels of untreated obstructive sleep apnoea syndrome (OSAS) resulting from ATH in children [1,3,12]. Adenotonsillectomy has also been widely accepted as the treatment of choice for cardiovascular abnormalities resulting from ATH [4e6,12]. In the 1950s, childhood OSAS was diagnosed mainly by cardiologists and endocrinologists when children presented in heart failure or severe growth impairment [5]. But currently, in the wake of increase awareness and higher frequency of AT for OSAS, majority of patients with ATH present with very mild symptoms or none, that relate to the cardiopulmonary system. However symptomless chronic cardiopulmonary changes may slowly occur in these children [6,12]. The more relevant questions are: whether milder forms of sleep disorder breathing in children are associated with cardiovascular changes, what factors influence the reversal of corpulmonale after AT, whether development of permanent pulmonary hypertension is dependent on the duration of upper airway obstruction before instituting AT treatment. In this present study, 39 cases were eligible for statistical analysis, out of which 43.6% had pulmonary hypertension. Incidentally we studied children whose cardiovascular changes were mild and not serious yet, and have not shown obvious abnormalities detectable on chest x-rays of our patients. All the PH in this study were mild with mPAP < 41 mmHg [13]. In the absence of detectable abnormalities on chest x-rays, early detection of cardiovascular abnormalities were easily done by monitoring mPAPs of our children with Doppler echocardiography. Most previous similar studies also reported studying children with mild cardiovascular changes in their series with mPAP of <40 mmHg [4e6,12,14]. In one study [15], it was reported that the mild form of cor pulmonale due to adenotonsillar enlargement could not be diagnosed clinically. In another study, Tal et al. [16] concluded that the right ventricular function may be compromised in children with obstructive sleep apnea even before the clinical signs of cardiac involvement are being detectable. Our study showed a significant reduction of mPAP postoperatively, with complete reversal of PH in more than 82% of the index cases. Similar results have been reported by other researchers. In one study [6], 51.9% of the eligible cases were reported to have PH although pulmonary hypertension was defined with
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Table 4 The extent of post-operative mPAP changes in relation to pre-operative measurements. Pre-operative parameters
Post-operative mPAP changes
P value
25% reduction Overall symptom score 7e10 points 5 >10 points 7 Adenoid nasopharyngeal ratio 0.75 8 >0.75 4 Tonsillar size (Brodsky grade) grades 1 & 2 2 grades 3 & 4 10 Pulmonary arterial pressure <25 mmHg 3 25 mmHg 9 Timing of adenotonsillectomy (in relation to onset of symptoms) <12 months 5 12 months 7
<25% reduction
Increased
4 21
1 1
*0.178
9 16
0 2
*0.033
5 20
1 1
* 0.554
17 8
2 0
*0.021
10 15
0 2
*0.743
*Fisher's exact test.
Table 5 Comparison of pre- and post-operative mean symptom scores n ¼ 39. Symptom domains
Pre-surgery mean score
Post-surgery mean score
Change score* (95% CI)
zP value
Overall symptom score Snoring Nocturnal mouth breathing Obstructive breathing during sleep Nasal obstruction Daytime stertor Daytime mouth breathing Daytime Hypersomnolence
8.5 1.7 1.4 1.6 1.4 1.3 1.1 1.2
3.1 0.5 1.0 0.2 0.9 0.2 0.7 0.8
5.4 1.2 0.4 1.4 0.5 1.1 0.4 0.3
0.000 0.000 0.021 0.000 0.012 0.000 0.001 0.037
(4.7e6.1) (0.9e1.4) (0.1e0.6) (1.2e1.6) (0.1e0.7) (0.9e1.4) (0.2e0.7) (0.2e0.6)
CI ¼ 95% Confidence interval, * ¼ pre-surgery mean minus post-surgery mean; z ¼ Paired sample t-test.
mPAP of 20 mmHg in contrast to our study where PH was defined by mPAP 25 mmHg. However, 67% of children with PH in the aforementioned study had normal mPAP values after AT, while the remaining 9 children were reported to have lower mPAP values compared with preoperative ones [6]. Abdel-Aziz [5] reported significant improvement of pre-operative cardiovascular parameters including mPAP. However the proportion of the cases with PH was not stated. Moreover there was relatively limited number of participants (18 children) in their study. Miman et al. [12] documented complete resolution of pre-operative echocardiographic pathologies, including normalization of mPAP in all the 18 patients with PH secondary to ATH, 3 month following AT. In contrast not all the children with PH in our study had complete reversal of their PH. As illustrated in Table 3, PH persisted in 3 of the participants at 6 week post-operative echocardiographic re-assessments. Although the number of unresolved PH seems too small for any conclusive statistical significance to be derived, non-resolution of PH seems to potentially correlated with gross adenoidal hypertrophy, as all of them were among the group of children who had ANR > 0.75 (P ¼ 0.043). However it was possible that our relatively shorter post-operative re-evaluation period of 6 weeks, (which was adopted in our study to minimise the potential loss of participants to follow up because of our socio-cultural peculiarities), might have accounted for the apparent non-resolution of PH. One may also speculate that suboptimal compliance or viral URT infections of these children during 2D echo measurement of mPAP, as well as incomplete resection of adenoid tissue or rapid re-growth/ enlargement of adenoid tissue may have played roles in these children. In a systematic review of the effects of AT on cardiovascular parameters in children with obstructive sleep apnoea Dawn et al.
[4] reported that out of the analysed 14 articles, 6 reported improvement in mean pulmonary artery pressures, 7 reported improvement in echocardiographic findings in general, after AT for OSAS. However they made the following observations: that there was none uniformity in the defining criteria for PH thereby making comparison difficult, and that none of the studies examined the correlation between the various cardiovascular parameters and OSAS severity. In this present study we attempted to evaluate whether the improvements recorded in the post-operative mPAP were related to symptom severity (symptom score), severity of adenoidal airway obstruction (adenoid-nasopharyngeal ratio), size of obstructive tonsils, duration of obstructive symptoms and the pre-operative mPAP values. We observed that significant reduction of mPAP (>25%) was significantly less likely to be encountered in children with gross adenoidal hypertrophy, but was more likely in those with pre-operative mPAP exceeding 25 mmHg. In other words, children with PH were more likely to have significant reductions of their pulmonary arterial pressure following AT than children with normal mPAP. However, the reduction of mPAP occurred after AT irrespective of the degree of pre-operative symptom severity, or duration of the symptoms before AT. The improvement did not also correlate with the size of the tonsils. Oran et al. [21] reported significant reversal of pulmonary hypertension among 20 children with different URT obstructions compared to 20 healthy controls after AT which supports our findings that PH is readily amenable to AT. However, similar to our data, Naigoblu et al. [22] reported that these observed significant reversal of PH occur regardless of the symptom severity. Our major limitation was our inability to perform a polysomnography which is the gold standard for diagnosis of OSA.
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However polysomnographic evaluation is not a routine clinical investigation. It is cumbersome to apply and is further compounded by its limited availability and additional cost. Unlike polysomnograghy that measures derangements in physiologic parameters during sleep; clinical evaluation focuses on the physical problems and functional limitations consequent on upper airway obstruction as reported by caregivers. However, predictive accuracy of clinically suspected OSAS may be as low as 30% when polysomnograghy testing was performed as well [17,18]. Nevertheless, standardised symptom grading has been shown to reliably evaluate the degree of upper airway obstruction by ATH in children [19,20]. In this present study the overall symptom score and the scores for all individual symptoms showed significant dramatic improvement after AT, which seem to correlate with the improvement in the mPAP. Moreover, the two children that showed no significant improvement in their symptoms also correspondingly showed persistence of their PH after AT. Our study was also limited by the relative low number of participants as well as the relative shorter follow-up period of 6 weeks which seems to be an early time point to figure out the exact resolution of pulmonary hypertension. In conclusion, PH due to ATH may be reversible by adenotonsillectomy. The reversal seems not related to the timing of the surgery or to the symptom severity, but the degree of mPAP improvement may be related to the radiological size of adenoid and the pre-operative mPAP. Cardiopulmonary status of children with ATH can readily be assessed by echocardiographic examinations and may be beneficial in taking useful decision before adenotonsilectomy and for assessing the benefit of surgery after AT. Conflict of interest None declared. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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