International Journal of Pediatric Otorhinolaryngology 78 (2014) 1381–1386 Prevalence and associated factors of pulmonary hypertension in Kenyan children with adenoid or adenotonsillar hypertrophy Diana Marangu a,*, Christine Jowi a, Joyce Aswani b, Sidika Wambani c, Ruth Nduati a aDepartment of Paediatrics and Child Health, University of Nairobi, Nairobi, Kenya bDepartment of ENT Surgery, University of Nairobi, Nairobi, Kenya cRadiology Department of Kenyatta National Hospital (KNH), Nairobi, Kenya A R T I C L E I N F O Article history: Received 14 January 2014 Received in revised form 29 May 2014 Accepted 5 June 2014 Available online 16 June 2014 Keywords: Adenoid hypertrophy Adenotonsillar hypertrophy Upper airway obstruction Pulmonary hypertension Kenya A B S T R A C T Objectives: Adenotonsillar hypertrophy is a common condition in childhood, whose serious complications of pulmonary hypertension and cor pulmonale are devastating but local prevalence is unknown. This study determined the prevalence and associated factors of pulmonary hypertension in children with adenoid or adenotonsillar hypertrophy at Kenyatta National Hospital, Kenya. Methods: This was a cross sectional hospital based survey conducted among children below 12 years of age with clinical and radiological adenoid hypertrophy attending the ear, nose and throat (ENT) outpatient clinic and general pediatric wards. Doppler echocardiography was used to determine pulmonary hypertension defined as a mean pulmonary arterial pressure (mPAP) of �25 mm Hg using the Chemla equation. Children with mPAP of �25 mm Hg were compared to those with lower pressures and clinical and radiological factors associated with pulmonary hypertension determined using multivariate logistic regression analysis. Results: Of the 123 eligible children in the study, 27 had pulmonary hypertension giving a prevalence of 21.9% (95% CI 14.64%–29.27%). Independent factors associated with pulmonary hypertension included nasal obstruction (OR = 3.0 [95% CI 1.08–8.44] p = 0.035) and hyperactivity on history (OR = 0.2 [95% CI 0.07–0.59] p = 0.003) and adenoid-nasopharyngeal ratio (ANR) >0.825 on lateral neck radiography (OR = 5.0 [95% CI 1.01–24.37] p = 0.048). Conclusion: One in five children with adenoid or adenotonsillar hypertrophy had pulmonary hypertension with a 3-fold and 5-fold increased odds in those with nasal obstruction on history and ANR >0.825 on lateral neck radiography respectively and an 80% reduced odds in reportedly hyperactive children. ã 2014 Elsevier Ireland Ltd. All rights reserved. Contents lists available at ScienceDirect International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier .com/ locate / i jpor l Introduction Adenotonsillar hypertrophy is a common condition in childhood and is the most common cause of upperairway obstruction and sleep disordered breathing in children [1]. Pulmonary hypertension and cor pulmonale are serious potentially fatal complications of upper airway obstruction [2]. Upper airway obstruction causes hypoxemia, hypercarbia and respiratory acidosis, all of which are potent vasoconstrictors of the pulmonary vasculature [3]. In the acute phase, pulmonary vasoconstriction is reversible if airway obstruc- tion is alleviated. However, chronic vasoconstriction results in structural remodeling of the pulmonary vascular bed and * Corresponding author. Tel.: +254 721282815. E-mail address:
[email protected] (D. Marangu). http://dx.doi.org/10.1016/j.ijporl.2014.06.002 0165-5876/ã 2014 Elsevier Ireland Ltd. All rights reserved. subsequently irreversible pulmonary hypertension and cor pulmo- nale ensue [3,4]. Globally, the prevalence of pulmonaryhypertension among children with adenoid or adenotonsillar hypertrophy varies widely between 7.3% and 51.9% based on echocardiography studies [5–8]. Annually there are over 6000 clinical contacts made with children with adenoid or tonsillar hypertrophy at the ear, nose and throat (ENT) outpatient clinic at the Kenyatta National Hospital (KNH), Nairobi’s leading referral health facility [9]. The objective of this study was to determine the prevalence of pulmonary hypertension in children with adenoid or adenotonsillar hypertro- phy at KNH, Kenya and secondarily determine clinical-radiological factors associated with pulmonary hypertension. Estimating the burden of pulmonary hypertension via echocardiography and identifying associated factors in these children in our setting allows for early clinical recognition of children at risk of pulmonary http://crossmark.dyndns.org/dialog/?doi=10.1016/j.ijporl.2014.06.002&domain=pdf mailto:
[email protected] http://dx.doi.org/10.1016/j.ijporl.2014.06.002 http://dx.doi.org/10.1016/j.ijporl.2014.06.002 http://www.sciencedirect.com/science/journal/01655876 www.elsevier.com/locate/ijporl 1382 D. Marangu et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 1381–1386 hypertension and their prioritization for appropriate and timely interventions such as adenoidectomy or adenotonsillectomy to prevent fatal sequelae. Materials and methods A hospital based cross sectional descriptive study was carried out within the ENT department and pediatric wards of KNH over a period of 4 months among children aged 0–12 years with clinician diagnosed adenoid hypertrophy with or without tonsillar hyper- trophy as the only cause of upper airway obstruction, confirmed on lateral neck radiography and had written informed consent from their guardians. Children were excluded from the study if they had neurologic abnormalities such as cerebral palsy, genetic syndromes with craniofacial abnormalities such as Down syndrome, or other causes of upper airway obstruction such as deviated septum, nasal polyposis, gross turbinate hypertrophy or a body mass index (BMI) >95th percentile for the age. Gross inferior turbinate hypertrophy in this study was defined as complete occlusion of the nasal cavity (Grade III according to Friedman et al.) on either the left or right side [10]. Children were also excluded if they had other co- morbidities known to be associated with pulmonary hypertension such as a known diagnosis human immunodeficiency virus (HIV), sickle cell anemia, chronic lung disease, cardiac disease or cardiac disease discovered on echocardiography that could otherwise explain the pulmonary hypertension. In addition, children whose caregivers refused to grant written informed consent or for whom echocardiography was not performed were excluded. Upon enrollment, history was obtained from the caregivers and physical examination performed on all children comprising a general, ENT and cardiovascular evaluation. Grading of tonsil size on physical examination employed the Brodsky classification [11]. Lateral neck radiography was performed in the KNH radiology department using a standardized technique and image quality was assessed. Good quality image was defined as one without rotation or magnification and was taken with the mouth closed. A diagnosis of adenoid hypertrophy was made by any hospital clinician if a child had suggestive symptoms or signs of upper airway obstruction confirmed as adenoid hypertrophy on lateral radiography by any hospital radiologist and had tonsil grade 0–2 on physical examination assessed by the study clinician using the Brodsky classification. A diagnosis of adenotonsillar hypertrophy was made by any hospital clinician if a child had suggestive symptoms or signs of upper airway obstruction confirmed as adenoid hypertrophy on lateral radiography by any hospital radiologist and tonsil grade 3 or 4 on physical examination assessed by the study clinician using the Brodsky classification [11]. The anterior nasal examination was conducted by the study clinician by visual inspection using a head lamp as a light source. Children without Grade III inferior turbinate hypertrophy accord- ing to the Friedman classification (i.e., those with Grade I – mild nasal obstruction; and Grade II – between Grade I and Grade III) were included and the analysis was conducted on these children as a combined group [10]. The radiographs were reviewed by a pediatric radiologist who was blinded to the severity of the patients’ disease. Adenoid size, nasopharyngeal size, tonsil size and pharyngeal size were measured in centimeters to the nearest decimal point with a ruler and the adenoid nasopharyngeal ratios (ANR) and tonsil pharyngeal ratios (TPR) were determined using a standardized technique proposed by Shintani [12]. In the literature an ANR cut- off of >0.63 has been used as a criteria for enlarged adenoids on lateral neck radiography although this was not used as a criteria for inclusion in our study [13]. An ANR cut-off of 0.825 was an arbitrary cut-off taken in this study that is between 0.63 and 1, as all children in our study had an ANR >0.63. Granzotto et al. previously reported a TPR cut-off of >0.66 on lateral neck radiography to be a predictor of pulmonary hypertension in children with adenoid hypertrophy [7]. These various cut-offs were used to report measurements taken on lateral neck radiography for our study patients. Echocardiography was performed by the pediatric cardiolo- gist who was also blinded to the severity of the patients’ disease. Transthoracic M-mode, 2D echo and Doppler echocardiography were carried out using a portable VIVID I Echo Color Ultrasound System echocardiography machine. Cardiac measurements were performed according to the guidelines of the American Society of Echocardiography [14]. Systolic pulmonary artery pressure (sPAP) was measured and the modified Bernoulli equation applied using the tricuspid regurgitation jet [15]. Mean pulmo- nary artery pressure (mPAP) was then derived using the Chemla equation = (0.61 � sPAP) + 2 mm Hg [16]. Estimated mPAP using the Chemla equation has been shown to have an acceptable accuracy of 77–98% within 10 mm Hg of right heart catheteriza- tion measured mPAP and thus suitable for clinical use [17]. In addition, an estimated mPAP � 25.5 mm Hg using the Chemla equation is useful in the diagnosis of pulmonary hypertension with an excellent sensitivity (98%), specificity (100%), positive (98%) and negative (88%) predictive value [18]. Pulmonary hypertension was defined as an estimated mPAP of �25 mm Hg [15]. Digital images and videos of the echocardio- graphs were stored for future validation. During the procedure young infants were pacified with breastfeeding or distracted with toys. Light sedation with oral chloral hydrate at a dose of 25 mg/kg/ dose was administered when needed. Ethical approval was sought from Kenyatta National Hospital Scientific and Ethics Committee and the study was performed in accordance with the guidelines of the Declaration of Helsinki. Statistical analysis Data were entered in a preformed Microsoft Access database and analysis performed using STATA version 12.0. Chi square test of association or Fisher’s exact test where appropriate were used to compare categorical variables and an odds ratio was reported to give an estimate of risk. Student’s t-test was employed when means were compared and Mann–Whitney U test was used to compare medians. A multivariate logistic regression analysis was conducted with the main outcome as presence or absence of pulmonary hypertension. Results From September to November 2012, a total of 127 children meeting study eligibility criteria were enrolled of whom 123 completed the required echocardiography evaluation and qualified for further analysis. As shown in Table 1, the median age of the study population was 2.5 years, with a male to female ratio was 1.5:1. Overall, 94.4% of the study participants were well nourished with weight for height Z-scores >�2 with only six (4.8%) moderately wasted and one (0.8%) severely malnourished. The median duration of symptoms suggestive of upper airway obstruction was 14 months, ranging from 1 to 60 months and 93 children out of 123 (75.6%) were on intranasal steroids. Majority of the patients 115 out of 123 (93.5%) were recruited from the ENT clinic. Only 39 out of 123 (31.7%) were scheduled for corrective surgery. The commonest symptoms reported by guardians of the 123 study participants were frequent upper respiratory infection (URTI) by 119 (97%), snoring 118 (96%), restless sleep 111 (90%) and frequent awakening 99 (80%). Moderately frequent reported Table 1 Patient characteristics in children with adenoid or adenotonsillar hypertrophy at KNH (N = 123). Characteristic Frequency (%) Sex Male 74 (60) Age in years (Median (IQR) [Range]) 2.5 (1.4–3.5) [03–85] Weight for height z score (WHZ) �2 116 (94.3) Duration of symptoms in months (Median (IQR) [Range]) 14 (2–51) [1–60] Use of intranasal steroid 93 (75.6) Surgery scheduled 38 (30.9) Recruitment from ENT outpatient clinic 115 (93.5) Clinical symptoms Snoring 118 (96) Pauses 56 (46) Restless sleep 111 (90) Frequent awakening 99 (80) Night sweats 93 (76) Mouth breathing 80 (65) Nasal obstruction 62 (50) Frequent URTI 119 (97) Hyperactivity 79 (64) Enuresis (age > 4 years) 9 (7) Clinical signs Hypoxia 4 (3) Tachypnea 3 (2) Tachycardia 14 (11) Palpable P2 18 (15) Murmur 4 (3) Hepatomegaly 3 (2) Edema 4 (3) Mouth breathing 92 (75) Predominant adenoid hypertrophy (Brodsky tonsil size 0–2) 56 (46) Predominant adenotonsillar hypertrophy (Brodsky tonsil size 3–4) 67 (54) Lateral neck radiography Adenoid pharyngeal ratio >0.63 on lateral neck radiography 123 (100) Tonsil pharyngeal ratio >0.66 on lateral neck radiography 41 (33) Good image quality 19 (15) Normal pu Borderline Pulmonary 3 21.9% ulmonary pre e elevated pre y hypertensio 4 36.6% % ssures : mP AP essure s: mP A on: mPA P ≥ 25 41.5% P 20mmHg 5mmHg 0.63 on lateral neck radiography and only 36 out of 123 (29%) children in the study had a tonsil pharyngeal ratio >0.66. Good image quality was reported in 19 out of 123 (15%) as shown in Table 1. Twenty-seven children of the 123 (21.9%) study participants had mean pulmonary pressures �25 mm Hg and therefore classified as having pulmonary hypertension. The point prevalence of pulmonary hypertension was 22% (95% CI 14.6–29.2), as illustrated in Fig. 1. Forty five children out of 123 (22.3%) had borderline elevation of mPAP >20 mm Hg but Table 2 Factors associated with pulmonary hypertension in children with adenoid or adenotonsillar hypertrophy at KNH (N = 123). Risk factors No Pulmonary hypertension N = 96 (%) Pulmonary hypertension N = 27 (%) Odds ratio (95% CI) p value Patient characteristics Age in yearsa Median (IQR)a 2.6 (0.8–7.2) 1.8 (0.5–4.3) – 0.04 Sex (male) 54 (56.2) 20 (74.0) 2.2 (0.86–5.75) 0.1 WHZ score ( 4 years) 6 (6.32) 3 (11.1) 1.85 (0.43–7.96) 0.4 Clinical signs Hypoxia 2 (2) 2(7.4) 3.76 (0.50–28.03) 0.2 Tachypnea 1 (1) 2 (7.4) 7.60 (0.66–87.24 0.1 Tachycardia 12 (13) 2 (7.4) 0.56 (0.12–2.67) 0.7 Palpable P2 8 (8) 10 (37.0) 6.47 (2.23–18.77) 0.001 Murmur 3 (3) 1 (3.7) 1.19 (0.12–11.95) 1.0 Hepatomegaly 0 (0) 3 (11.1) 1 0.01 Edema 1 (1) 3 (11.1) 11.9 (1.18–119.28) 0.03 Tonsil size [Brodsky grade 3–4] 49 (51.0) 18 (66.7) 1.9 (0.78–4.69) 0.2 Mouth breathing 68 (70.8) 24 (88.9) 3.3 (0.92–11.83) 0.08 Lateral neck radiography Adenoid size (cm)c 2.10 2.39 – 0.04 ANR >0.825 67 (69.8) 25 (92.6) 5.4 (1.2–24.4) 0.02 Tonsil size (cm) Median (IQR)b 0.8 (0.0–2.0) 0.56 0 (0.0–1.4) 0.08 TPR >0.66 34 (35.4) 7 (25.9) 0.64 (0.25–1.66) 0.4 a Wilcoxon–Mann–Whitney test. b Fisher’s exact test. c Student’s t-test. 1384 D. Marangu et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 1381–1386 (70%) of 27 versus 43 (45%) of 26, OR = 2.9 [(95% CI 1.17–7.34), p = 0.019]. Guardians of children with pulmonary hypertension had reduced likelihood of reporting hyperactivity 9 (33%) of 27 versus 70 (73%) of 96, OR = 0.19 [(95% CI 0.07–0.47), p < 0.0001]. There was a trend to shorter duration of symptoms in children diagnosed with pulmonary hypertension 11 versus 15 months, p = 0.08. Guardians of children with pulmonary hypertension had a trend toward increased reporting of mouth breathing 22 (82%) of 27 versus 58 (60%) of 96, OR = 2.9 [(95% CI 1.01–8.27), p = 0.066] and night sweats 24 (89%) of 27 versus 69 (72%) of 96, OR = 3.1 [(95% CI 0.87–11.26), p = 0.080]. Snoring, restless sleep, frequent awakening, frequent URTI and enuresis at age >4 years were not associated with pulmonary hypertension. The clinical signs that were associated with pulmonary hypertension included presence of a palpable P2 (OR = 6.47 [95% CI 223–1877] p = 0.001) and edema (OR = 11.9 [95% CI 1.18–119.28] p = 0.033). Tonsil size Brodsky grade 3 and 4 and mouth breathing on physical examination were not associated with pulmonary hypertension. On examination of the lateral neck radiograph, children with pulmonary hypertension had a larger adenoid size 2.39 cm versus 2.10 cm, p = 0.035. Up to 25 (92.6%) of the 27 children with pulmonary hypertension had an adeno-nasopha- ryngeal ratio (ANR) >0.825 compared to 67 (69.8%) of 96 without pulmonary hypertension OR = 5.4 [(1.2–24.4), p = 0.02] a significant difference. In choosing parameters to fit in the logistic model those that were significant on bivariate analysis were included. Nasal obstruction and pauses on history were considered to be surrogates for upper airway obstruction and hence only nasal obstruction was retained as it had shown a more significant association on bivariate analysis. Adenoid size and ANR >0.825 reflected adenoid hypertrophy on lateral neck radiography therefore only ANR >0.825 was retained as it showed a more significant association on bivariate analysis. A multivariate logistic regression analysis was conducted with the model including age, none-use of intranasal steroids, nasal obstruction and hyperactivi- ty on history and ANR >0.825 on lateral neck radiography. Cardiovascular parameters were not included in this model as these are established signs of pulmonary hypertension. In this study population, independent factors associated with pulmonary hypertension included history of nasal obstruction (OR = 3.0 [95% CI 108–844] p = 0.035), hyperactivity (OR = 0.2 [95% CI 0.07–0.59] p = 0.003) and ANR >0.825 (OR = 5.0 [95% CI 1.01–24.37] p = 0.048) as shown in Table 3. Age and non-use of intranasal steroids were not associated with pulmonary hypertension. Discussion The point prevalence of pulmonary hypertension among children with adenoid and adenotonsillar hypertrophy was 22% (95% CI 14.6–29.3). That means 1 in 5 children with clinician diagnosed and radiologically confirmed adenoid or adenotonsillar hypertrophy at KNH from September 2011 to December 2011 had pulmonary hypertension. With over 6000 clinical contacts Table 3 Independent factors associated with pulmonary hypertension in children with adenoid or adenotonsillar hypertrophy at KNH (N = 123). Risk factors Odds ratio (95% CI) P value Patient characteristics Age 1.0 0.78–1.33 0.902 Intranasal steroid none–use 1.6 0.52–4.87 0.409 Clinical symptoms Nasal obstruction 3.0 1.08–8.44 0.035 Hyperactivity 0.2 0.07–0.59 0.003 Lateral neck radiography ANR >0.825 5.0 1.01–24.37 0.048 Multivariate logistic regression. D. Marangu et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 1381–1386 1385 annually at the ENT outpatient clinic, there are an estimated 1200 children having pulmonary hypertension and at risk of cor pulmonale [9]. Globally, there has been a lack of standardizations on methods used in studies evaluating pulmonary hypertension in children with adenoid or adenotonsillar hypertrophy on echocardiography with regard to differences in cut-off points defined for pulmonary hypertension, equations used to derive mean pulmonary arterial pressures as well as patient selection [5–8]. Notwithstanding these differences, the prevalence of pulmonary hypertension elicited in this study is up to 4 times higher when compared to that reported in other studies and only similar to the Turkish study of 2004 by Yilmaz et al. when data is compared head to head [5]. Although altitudes of cities in which these studies have been undertaken vary, none of them meet the high altitude criteria of above 2500 m above sea level which is associated with pulmonary hypertension [15]. Afyonkarahisar in the Turkish study by Yilmaz lies at 1020 m above sea level. The altitudes of cities in which other studies referenced were conducted range from 37 to 1800 m above sea level. This study was conducted in Nairobi which lies at about 1680 m above sea level. Only 2 children in the study with pulmonary hypertension lived in towns outside Nairobi (Kericho and Kijabe at 1982 m and 2200 m above sea level, respectively). The authors postulate that racial and genetic differences may contrib- ute to observed variations. Thirty three children out of 123 (27%) had mean pulmonary arterial pressures >20 mm Hg but 0.63 to be at a higher risk of cardiopulmonary complications when compared to those with ANR 0.63 was not associated with pulmonary hypertension in children in our setting. However this study shows that an ANR >0.825 is associated with pulmonary hypertension. The research team did not find any published data on this ANR cut-off as a predictor of pulmonary hypertension. This is however biologically plausible as the greater the adenoid tissue in relation to the nasopharyngeal spacethenthegreater theupperairwayobstruction. This study is useful for clinicians in similar settings in that it provides both clinical and radiographic parameters to objectively identify children with pulmonary hypertension and therefore initiate prompt management. These parameters include a history of nasal obstruction as well as an ANR cut-off of >0.825 on lateral neck radiography. The utility of the absence of reported hyperactivity being a new finding needs to be explored further in future studies. Limitations of this study include selection bias which may have occurred as patients without lateral neck radiographs were excluded. Nonetheless, the children attending the ENT outpatient clinic during the study period were comparable with the children in our study with regard to age and sex. Despite standardization of the radiography technique, few radiographs were of good image quality, a common occurrence in lateral neck radiography in children however measurements taken have been shown in this study to have utility. An additional constraint is the lack of data of normal pulmonary pressures in children for age, sex, body mass index and geographical variation in our setting to truly cater for differences if any. Finding an ideal control group of children seeking care in this tertiary health facility was challenging. We attempted to mitigate this limitation by excluding children with other co-morbidities that could otherwise explain the pulmonary hypertension such as a known diagnosis human immunodeficien- cy virus (HIV), sickle cell anemia, chronic lung disease, cardiac disease or cardiac disease discovered on echocardiography. Conclusion In conclusion, pulmonary hypertension was present in 1 in 5 children with adenoid or adenotonsillar hypertrophy at KNH and was more likely in children who presented with a history of nasal obstruction, no hyperactivity and had an ANR >0.825 on lateral neck radiography. 1386 D. Marangu et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 1381–1386 Conflict of interest None. References [1] R. Bhattacharjee, L. Kheirandish-Gozal, G. Pillar, D. 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