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DISORDERED BREATHING DURING SLEEP IN NEWBORNS, INFANTS, AND CHILDREN
0030-6665/99 $8.00 + .OO
SLEEP APNEA, PART I1
DISORDERED BREATHING DURING SLEEP IN NEWBORNS, INFANTS, AND CHILDREN Symptoms, Diagnosis, and Treatment Jack Coleman, MD
Disordered breathing during sleep is thought to have an incidence of around 3% in the pediatric age group. It has been known that there is a correlation with behavior and learning problems and sleep disorders for at least 100 years.I2It is well-known that the term for pickwickian syndrome comes from Charles Dickens’ description of the hypersomnolent lad in Posthumous Papers of the Pickwick Club. With the advent of polysomnography, these disorders could be defined better in the pediatric age group and the result of this further investigation has been the discovery of considerabledifferences in sleep disorders involving newborns,infants, and children versus adults. The respiratory tract, like any other body system, undergoes growth and development from birth to adulthood. This is reflected not only in anatomic changes in the structure of the airway, but also in the neurologic function and control of the airway. It is not uncommon to note irregular breathing patterns in neonates and infants. The question that arises is whether these irregular breathing patterns are benign and will improve as the airway develops, whether this represents normal physiology, or whether these are potentially lifethreatening periods. Four reasons have been described for the difference in respiratory physiology between premature and term infants and that of the adult.20First, the neural network in the brainstem that is responsible From the Nashville Ear, Nose and Throat Clinic, Nashville, Tennessee OTOLARYNGOLOGIC CLINICS OF NORTH AMERICA VOLUME 32 *NUMBER 2 * APRIL 1999
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for the initiation and control of ventilation is not completely developed at this point so that the pattern of neural activity will be different from that of the adult. Second, there is a difference in sensitivity to chemoreceptors and subsequent brain activity that is age dependent. The typical response of an infant to hypoxia will be biphasic in that one initially will see hyperventilation followed by depressed ventilation. Third, in the infant respiratory rate can be decreased by afferent impulses from the upper airway. And fourth, the coordination between the postcricoarytenoid muscle responsible for opening the glottis and the diaphragm muscle is not developed fully, resulting in episodes where the airway is not opening to allow entrance of air with contraction of the diaphragm. Therefore, the child will be trylng to breathe against a closed glottis. The result of this is that neonates are likely to have irregular respiratory rates compared with the adult, and brief apneas in this age group are very common. Over the first few months of life this becomes less and less of a problem as the child develops. There are also simple anatomic problems or differences between the airway of the neonate and that of the older child or adult. The airway lumen itself is much smaller. The respiratory rate is also much higher. Neonates are said to be obligate nose breathers, and although one finds this is true in most instances, there are times when one finds children with bilateral choanal atresia who are able to survive initially until this diagnosis is made and treatment is started. There are also variations in the sleep/wake pattern in that infants frequently do not have a set pattern and it may take some time for a circadian rhythm to develop. Lastly, there are differences in basic respiratory physiology between the infant and the adult. In children who suffer from obstructive sleep apnea syndrome, there are some common features shared with the adult as far as the nature of the obstruction and its ability to be measured, and also some of the anatomic features. There is a significant difference in the symptomatology that the patient may suffer as a child, however, as well as significant differences in the treatments available and methods of diagnosis. In children, as with neonates, some central apneas may be found and may be perfectly normal. These periods would be considered abnormal, however, if on polysomnogram they were found to cause bradycardia or significant oxygen desaturations. This would be indicative of an inborn disorder of respiratory control that would require treatment. CAUSES OF OBSTRUCTIVE SLEEP DISORDERED BREATHING
There are many causes of obstructive sleep disordered breathing found in the pediatric age group that may not be found in the adult age
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group (Table 1).As in adults, obstructive apnea more commonly occurs because of upper airway obstruction; there may be significant lower airway compromise, however, because of vascular rings, tracheal webs, atresias, and goiter. The primary goal in treating these children is first to find out what the cause is and from there determine appropriate therapy. Sleep disordered breathing in children, as with adults, can be due to central Table 1. SOME OF THE CAUSES OF OBSTRUCTIVE SLEEP DISORDERED BREATHING IN INFANTS AND CHILDREN Anatomic
Upper airway Deviated septum Nasal polyps Enlarged turbinates Choanal stenosis or atresia Macroglossia Hypertrophy of tonsils and adenoids Micrognathia Epignathia Temporomandibular joint ankylosis Lower airway Laryngeal and tracheal webs Tracheal atresia Intrinsic tracheal lesions Extrinsic compression (goiter) Laryngotracheomalacia Congenital
Apert‘s syndrome Cri du chat syndrome Crouzon syndrome Down syndrome Nager’s syndrome Pierre Robin syndrome Prader-Willi syndrome Treacher Collins syndrome Cystic fibrosis Mucopolysaccharidoses (Hunter’s and Hurler’s syndromes) Juvenile rheumatoid arthritis Cerebral palsy Chiari malformation Cranial basal malformations Craniofacial microsomia Pharvngeal encephalocele Other
Myopathy Neuromuscular disease Neoplasm Familial factors Gastroesophageal reflux
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or obstructive phenomena or a combination of the two. Brief periods of central apnea can be common in infants and frequently are seen in children. This sometimes is referred to as idiopathic apnea or apnea of prematurity or apnea of infancy, depending on whether the child is premature or term. Before making this diagnosis, however, one must rule out infection, obstruction, seizure disorders, or other metabolic problems as a cause for a central apnea. Congenital central alveolar hypoventilation, otherwise known as Ondine's curse, may show long periods of central apnea." This disorder, if undiagnosed, has a very high mortality rate and even when diagnosed, may prove very difficult to control. Treatment usually requires some type of ventilatory assistance for the patient and various devices have been used successfully for this. Obstructive sleep apnea may be caused by the same disproportionate anatomy as found in adults. In addition to this, it also may be because of impaired coordination of the muscles in the respiratory tract, especially between the diaphragm and dilators of the respiratory tract, and also because of congenital anomalies, both anatomic and neurologic. Some of these anomalies may be immediately life-threatening in the neonate and require prompt treatment as a life-saving measure. In the first few days of life to 6 weeks of age, upper respiratory infections are the most common causes of obstructive apnea. This is because of a combination of copious secretions and small airway diameter and inability to clear the secretion. In older infants and children, large adenoids and tonsils are the most common reason for obstructive sleep apnea. This may be seen in relation to mucopolysaccharidoses or sickle cell disease.I7 Although obstructive apnea in children is generally a peripheral disturbance, it also may reflect a central brainstem dysfunction.' This may cause hypotonia to severe spasticity, including the muscles of the airway such as the tongue and vocal cords. Abnormal posturing and poor head control may obstruct the airway, as will poor swallowing, which would allow for sigruhcant buildup of secretion. When surgical treatment such as adenotonsillectomyis performed on these patients, one may see a transient worsening of these conditions because of the tendency to increase pooling because of decreased swallowing from pain and the effects of analgesic medications on the patient. Obstructions also may be complete or incomplete as in adults, and children with these problems may do much better when awake and worse with sleep and muscle relaxation. This may lead to significant changes during rapid eye movement (REM) sleep when there are maximal degrees of atonia. Obesity would appear to be a less frequent cause of airway obstruction in children, and this will be discussed later in the article.
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SYMPTOMS, SIGNS, AND THE EFFECTS OF SLEEP APNEA ON CHILDREN
In infants, apnea may manifest itself with metabolic alkalosis, and repeated episodes of severe apnea actually may cause asphyxia1 brain damage. Obstructive apnea and central apnea have been implicated as possible etiologies for sudden infant death syndrome (SIDS). In children the blood chemistries actually may show a metabolic acidosis, and repeated episodes of apnea may result in developmental delay^.^ One of the major differences between the adult apneic patient and the child is with weight. Whereas in the adult obesity is a common finding in sleep apnea, in children 27% will show failure to thrive. In those with a normal weight range, one third of the children will have some type of underlying facial deformity or neuromuscular disorder. It is felt that the inability to gain weight is due to several reasons. First are the changes that occur in a child’s behavior secondary to the disturbed sleep. Second, because of adenoid enlargement there usually is a decreased sense of smell, and eating is not particularly enjoyable to the patient; therefore, he or she tends not to eat as much. Also, it is very difficult for the child to swallow when the upper airway is significantly obstructed by the mass of the tonsils and adenoids. The child is unable to eat and breathe at the same time. Often their food preference is to very soft foods or liquids. It takes them quite a long time to get a meal down, sometimes longer than the parents are willing to give them. They also gag and choke easily and food will tend to stick in their throat, making adequate nutrition very difficult for these children. One also may see polycythemia in these children as in adults, along with systemic hypertension that may lead eventually to cor pulmonale. It is estimated that cor pulmonale is present in 25%of children with obstructive sleep apnea ~yndrome.~ During the daytime these children are frequently irritable, aggressive, hyperactive, and are discipline problems. Many children who have been placed on methylphenidate HC1 and are diagnosed as having hyperactivity or attention deficit disorders in fact suffer from sleep disorders. Many of these children will complain of early morning headache due to carbon dioxide retention. Their memory frequently is impaired, as is their concentration, and school performance subsequently will suffer because of this. Their behavior also may cause significant interferencewith a normal family life. In teenagers, excessive daytime sleepiness may lead to significant hypersomnolenceand motor vehicle accidents while driving. At nighttime, these children have significant snoring in almost 100% of cases, interrupted by periods of silence. They are very restless sleepers and tend to sleepwalk at night. Their sleep frequently is disturbed by bad
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dreams and nightmares. They tend to sleep with their head extended in order to open the pharyngeal airway as much as possible. Because of their hyperactivity during sleep, they frequently are diaphoretic, as well. Enuresis also may be a problem in these children; care must be made, however, in assigning this symptom to the child, and attention must be paid to his or her age and what is considered normal onset of bladder control at night. On examination the various congenital anomalies that have been found to be causative factors may be apparent readily to the physician. In addition, one may notice some hyponasal speech. As patients get older, they may develop adenoid facies or elongation of the midface from mouth breathing, as well as an open bite deformity as a result of their chronic attempt to adjust their airway to circumvent the obstruction. They also may develop a pectus excavatum as a result of chronically breathing against resistance at night. This may be aggravated in cases of partial daytime obstruction, as well. Some children will be frankly pickwickian, which will be notable in the waiting room or examination room. TESTING
As in adults with obstructive sleep disorders, testing is essential to making the diagnosis. The predictive value of a good history and physical examination by a physician familiar with sleep disorders in comparison to diagnosis made on polysomnogram is between 30% to 50%.23Of significance is that frequently adenotonsillectomyis performed based solely upon the symptomatology described by an observer and physical examination, and no testing is done on the patient. This would lead one to conclude that there may be a considerable number of adenotonsillectomies being performed for upper airway obstruction and sleep apnea that need not be done. In the same study, it was found that the symptoms with the highest predictive value were enuresis at 46% and snoring intensity of greater than 30 dB with a value of 60%. One of the major problems with polysomnography in children is that there is no well-defined demarcation between what is considered a normal and abnormal polysomnogram in this age group. One study states that the polysomnogram (PSG) is abnormal if the respiratory disturbance index is greater than 5.1° Another study has abnormal parameters of a respiratory disturbance index (RDI) of greater than 15 per hour, or 25 per hour for 1 hour.9 And yet another study defines an abnormal polysomnogram as an RDI greater than 1,0, saturations dropping below 92%, end tidal CO, of greater than 53 mm Hg, and hypoventilation duration greater than 60%.16
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Sleep somnography or recording of the snoring while the patient is asleep has been correlated with polysomnogram and does seem to have some predictive value as to the degree of apnea in patients with enlarged tonsils and adenoid^.'^ This technology is not able to differentiateobstructive apneas from central apneas, however. Endoscopy is also a useful tool in an attempt to determine sites of obstruction and to visualize what type of obstruction one may be dealing with, bearing in mind that congenital abnormalities or masses within the airway such as encephaloceles, laryngoceles, and so forth, although rare, may be a more common finding in children than in adults. Cephalometricradiographs and other imaging techniques are important to look at soft tissue anatomy, bony anatomy, and airway space. These are particularly important if surgical intervention, especially to the skeletal structures, is to be contemplated. Chest radiographs also may reveal an enlarged heart as a sign of chronic upper airway obstruction. Other tests also may provide useful pieces of information.Hematocrit may reveal polycythemia, arterial blood gases may reveal hypoxemia or hypercarbia, electrocardiograms (ECGs) and echocardiograms are useful to evaluate the heart, looking for possible right heart strain, and pulmonary function tests sometimes may show a saw-toothed pattern on flow volume loops, frequently seen with upper airway obstruction.
TREATMENT
The basic philosophy for treatment in the pediatric age group is to (1) eliminate or control the etiology of the obstructive breathing and (2) prevent episodes of serious breathing problems and their frequencyin order to decrease the risk of sequelae to repeated episodes of apnea. Treatment modalities can be divided into behavioral, medical, use of appliances, and surgery. Typical behavioral modifications are to decrease weight and try to improve sleep hygiene in the older child. In the neonate and infant, one tries to establish a regular sleep schedule. In addition, the physician should take a careful history of medication and drug use. In many patients, medications that have a sedative side effect may be used. Typical in younger children would be over-the-counter cold preparations being given before bedtime. In the older pediatric patient, one must consider drug use and alcohol use that may be causing aggravation of apnea. These histories sometimes may be very difficult to elicit, especially in the presence of a parent. Medical treatment may be used to treat factors aggravating or causing apnea or attempting to treat the apnea itself. Medical treatment of allergies
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and rhinitis is important, especially in the younger children with a smaller airway; one should avoid sedating antihistamines,however. Gastroesophageal (GE) reflux has the ability to increase the severity and number of apneas in a patient, and this should also be brought under control. If there is a question of reflux being present, appropriate diagnostic testing may need to be part of the work-up for the sleep disorder. There are medications that have been tried to control obstructive breathing disorders at night. Respiratory stimulants have not seemed to work very well. Protriptyline has been helpful in a few cases, but has not had consistent There are various devices available that will help control the apnea or alert the parent to significant apnea episodes. Continuous positive airway pressure (CPAP)long has been known to be an effective control measure for apnea in adults and is effective equally in children. In adults, the biggest problem has been with compliance with the use of the machine. In children, however, this is not as problematic as there is frequently parental supervision to ensure that the patient is compliant with the use of the apparatus. Dental appliances also have been used. Again, they do have a place in the treatment of the pediatric patient, especially in the course of treating patients with skeletal or dental problems contributing to the obstructive phenomena. Monitors are also useful in detecting significant apneas. Cardiorespiratory monitors are the most common type used and are more useful for central apnea than for obstructive sleep apnea. They should not be considered always as treatment devices. Pulse oximeters also fall into this category. Again, they basically are alerting and recording devices rather than actual treatment devices. Surgery has been the most common form of treatment in the pediatric age group and probably the most successfulform of treatment for obstructive breathing disorders for this patient population. Nasal surgery is necessary in some patients and the type of surgery depends upon what manner of obstruction one is dealing with. Septoplasty for deviated septums has been useful; because of concern for disruption of growth centers, however, a more conservative approach is taken in the younger age group than would be taken in adults. This procedure has been useful especially in children with a cleft lip or palate that frequently will have nasal obstruction on the side of the cleft. Nasal polyps can occur in the pediatric age group and may have to be removed in order to provide adequate airway. This commonly is needed in patients with cystic fibrosis. The nostrils may be narrow congenitally, and widening of the nostrils may have to be undertaken or even reconstruction of a nostril is needed in some craniofacial anomalies. Turbinates can become hypertrophied in allergy patients and the sue may need to be reduced. In the nasopharynx, one may have to correct a choanal atresia or choanal ste-
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nosis. One always must bear in mind that a nasal mass or nasopharyngeal mass may be originating from the central nervous system and an appropriate work-up should be taken prior to such excision. Adenotonsillectomy is the most common procedure performed in the pediatric age group for obstructive breathing disorders during sleep. It has been found to be effective 90% of the time when there is absence of craniofacial or neurologic abnormality.IO Even in cases of severe apnea where cox pulmonale may be present, there is usually prompt resolution of the symptomatology in the postoperative periodJ2 When treating the patient with adenotonsillectomy certain precautions must be taken that normally would not be taken in treating a patient with adenotonsillectomy for infectious etiology. Remembering the effects of the anesthetic and analgesic, there is the potential for temporary worsening of the symptoms in the immediate postoperative period and the airway must be monitored closely for this reason. Therefore, these procedures should not be done on an outpatient basis, but rather at least with an overnight stay and, in more severe cases, observation in an intensive care unit or stepdown setting. The patient should never be extubated until fully awake and able to guard the airway. Frequently, a nasopharyngeal airway is a useful adjunct in the recovery period. In some patients with significant hypopharyngeal airway compromise, an anterior tongue stitch is useful. One also should bear in mind that a patient may have more than one sleep disturbance and the physician should not develop a false sense of security that the patient has been cured by the adenotonsillectomy. Hypersomnolence, narcolepsy, or central apnea may exist still after the surgery and it is important that follow-up studies are performed to ensure that the sleep disorder has been treated adequately. It is especially true if there has not been adequate resolution of the symptoms. In some children with cleft palate, it has been shown that velopharyngeal flaps that have been used to treat velopharyngeal insufficiency may cause significant obstruction to the airway during ~1eep.I~ In these situations these flaps may need to be revised, or when the patient is older, if possible, completely taken down. Uvulopalatopharyngoplasty is performed in the pediatric age group, but not with the frequency that it is performed in the adult age group. Generally when it is performed, it is done in a more conservative fashion, especially with regard to resection of the midportion of the palate. If this procedure is done in conjunction with adenotonsillectomy, extreme caution must be taken as it has been shown that adenoidectomy performed in conjunction with a uvulopalatopharyngoplasty is one of the risk factors for development of significant nasopharyngeal inlet stenosis in the postoperative period.I4 Glossopexy also has been used in neonates and in patients with Pierre Robin syndrome. PSG indications have been devised by Freed et a17for this procedure. It is a reversible procedure when the airway has been
stabilized. In older patients requiring this procedure, the lower incisors may need to be removed in order to prevent breakdown of the site. Tracheotomy also is used in the pediatric age group. It probably is used more commonly in neonates and infants than in older children. As with adults, it does work quite well. Besides the usual problems seen with adults, however, there also are problems seen with its effects on language development and, in the older child, the psychosocial problems that arise from having a tracheostomy." Skeletal surgery, apart from that performed to correct congenital skeletal malformations, also is useful in carefully selected patients. By age 4, craniofacial growth is usually 60% of adult size and continues on to approximately age 16 in females and age 19 in males. When considering this type of surgery, one must try and determine whether the child will get better as he or she gets older and the facial bones grow in order to determine how aggressive one must be. There is some reluctance to do genioglossus advancements and hyoid myotomies, as well as bimaxillary advancement surgery in this age group, because of its potential effects on bone growth centers. Skeletal expansion surgery, however, has been shown to be quite useful in combination with soft tissue surgery in treating patients with craniofacial deformities? As mentioned, postoperative patients being treated for obstructive breathing disorders should be monitored closely. This is true especially in the younger patient, those with increased numbers of obstructive events on polysomnogram, patients in the lower percentile for weight and age, and those with abnormalities on their ECGs or echocardiograms.18Approximately 23% of patients that were treated surgically for obstructive sleep apnea had intermittent or continuous desaturations down to 70% or less in the immediate postoperative period. One also should remember that the effect of anesthetics and analgesics will increase airway collapse, and pediatric patients tend to have a decreased ventilatory response to elevated carbon dioxide 1e~els.I~ It also has been shown that postoperative pulmonary edema may ensue after relief of upper airway obstruction,and this can occur up to 12 to 14 hours postoperatively.8 In considering patients for surgical correction of their apnea, especially for adenotonsillectomy, one also should consider the degree of apnea. Patients with mild obstructive sleep apnea syndrome may get better spontaneously with age as the tonsils and adenoids regress in size normally. The treating physician also should make sure that the parents understand that the pathophysiology of obstructive sleep apnea in the child may be quite different from that in the adult, and that although adenotonsillectomy or other surgical interventions may cure the apnea in the child, there is a chance that as the patient gets older, apnea may reappear for different reasons.
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CONCLUSlON Although there are significant similarities in the process of obstructive breathing disorders in sleep in the pediatric age group in comparison to the adult age group, there also are some very significant differences. One must, therefore, take this into consideration when treating these patients, especially the smaller children, as these small airways are not terribly forgiving of errors in management. References 1. Arnold J, Allphin A. Sleep apnea in the neurologically impaired child. Ear Nose Throat J 7280-81,1993 2. Bonow M, St. John W, Bledsoe T Differential elevation by protriptyline and depression by diazepam of upper airway respiratory motor activity. Am Rev Respir Dis 1314-45, 1985 3. Brooks L: Treatment of otherwise normal children with obstructive sleep apnea. Ear Nose Throat J 72:77-79,1993 4. Brouillette R, Fernbach S, Hunt C: Obstructive sleep apnea in infants and children. J Pediatr 10031-40,1982 5. Brownell L, West P, Sweatman I, et al: Protriptyline in obstructive sleep apnea. N Engl J Med 307:1037-1042,1982 6. Cohen X, Ross D, Burstein F, et al: Skeletal expansion combined with soft tissue reduction in the treatment of obstructive sleep apnea in children: Physiologic results. Otolaryngol Head Neck Surg 119476-485,1998 7. Freed G, Pearlman M, Brown A, et a 1 Polysomnographic indications for surgical intervention in Pierre Robin’s sequence: Acute airway management and follow up studies after repair and take down of tongue-lip adhesion. Cleft Palate Craniofac J 25:151-155, 1988 8. Galvis A, Stool S, Bluestone C: Pulmonary edema following relief of acute upper airway obstruction. Arch Otolaryngol Head Neck Surg 80:112-128, 1980 9. Goldstein N, Sculerati N, Walsleben J, et a 1 Clinical diagnosis of pediatric obstructive sleep apnea validated by poIysomnogram. Otolaryngol Head Neck Surg 111:611-617, 1994 10. Guilleminault C, Korobkin R, Winkle R A review of 50 children with obstructive sleep apnea syndrome. Lung 159:275-287,1981 11. Guilleminault C, McQuitty J, Ariagno R, et a 1 Six infants with congenital alveolar hypoventilation syndrome. Pediatrics 70:684-697,1982 12. Hill W Some causes of backwardness and stupidity in children and the relief of these symptoms in some instances by nasophaqmgeal scarification. BMJ 2:711-712, 1889 13. Ingram R, Bishop J: Ventilatory response to carbon dioxide after removal of chronic airway obstruction. Am Rev Respir Dis 102:645-647, 1970 14. Katsantonis G, Friedman W, Krebs F, et al: Nasopharyngeal complications following uwlopalatopharyngoplasty. Laryngoscope 97:309-314,1987 15. Kravath R, Pollock C, Borowiecki B, et al: Obstructive sleep apnea and death associated with surgical correction of velopharyngeal insufficiency. J Pediatr 96:645-648, 1980 16. Marcus C, Carroll J, Coerne X, et al: Determinance of growth in children with obstructive sleep apnea syndrome. J Pediatr 125:556-562, 1994 17. Maddern B, Reed H, Ohen E, et al: Obstructive sleep apnea syndrome in sickle cell disease. Ann Otol Rhino1 Laryngol98:174-178,1989 18. McColley S, April M, Carroll J, et a1 Respiratory compromise after adenotonsillectomy in children with obstructive sleep apnea. Arch Otolaryngol Head Neck Surg 118:940943,1992
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19. Potsic W Comparison of polysomnogram and sonography for assessing regularity of respiration during sleep in adenotonsillar hypertrophy. Laryngoscope 971430-1437, 1987 20. Roloff D, Aldrich M: Sleep disorders and airway obstruction in newborns and infants in sleep apnea. Otolaryngol Clin North Am 23:639-650, 1990 21. Singer L, Kercsmar C, Legies G, et al: Developmental sequelae of long-term infant tracheostomy. Dev Med Child Neurol31:224-230,1989 22. Sofer S, Weinhouse E, Tal A, et al: Cor pulmonale due to adenoidal and tonsillar hypertrophy or both in children. Chest 93:119-122, 1988 23. Wang R, Elkins T, Keech D, et al: Accuracy of clinical evaluation in pediatric obstructive sleep apnea. Otolaryngol Head Neck Surg 118:69-73,1998 Address reprints requests to Jack Coleman, MD Nashville Ear, Nose and Throat Clinic Atrium Building Suite 200 250 25th Avenue North Nashville, TN 37203-1632
SLEEP APNEA, PART I1
DISORDERED BREATHING DURING SLEEP IN NEWBORNS, INFANTS, AND CHILDREN Symptoms, Diagnosis, and Treatment Jack Coleman, MD
Disordered breathing during sleep is thought to have an incidence of around 3% in the pediatric age group. It has been known that there is a correlation with behavior and learning problems and sleep disorders for at least 100 years.I2It is well-known that the term for pickwickian syndrome comes from Charles Dickens’ description of the hypersomnolent lad in Posthumous Papers of the Pickwick Club. With the advent of polysomnography, these disorders could be defined better in the pediatric age group and the result of this further investigation has been the discovery of considerabledifferences in sleep disorders involving newborns,infants, and children versus adults. The respiratory tract, like any other body system, undergoes growth and development from birth to adulthood. This is reflected not only in anatomic changes in the structure of the airway, but also in the neurologic function and control of the airway. It is not uncommon to note irregular breathing patterns in neonates and infants. The question that arises is whether these irregular breathing patterns are benign and will improve as the airway develops, whether this represents normal physiology, or whether these are potentially lifethreatening periods. Four reasons have been described for the difference in respiratory physiology between premature and term infants and that of the adult.20First, the neural network in the brainstem that is responsible From the Nashville Ear, Nose and Throat Clinic, Nashville, Tennessee OTOLARYNGOLOGIC CLINICS OF NORTH AMERICA VOLUME 32 *NUMBER 2 * APRIL 1999
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for the initiation and control of ventilation is not completely developed at this point so that the pattern of neural activity will be different from that of the adult. Second, there is a difference in sensitivity to chemoreceptors and subsequent brain activity that is age dependent. The typical response of an infant to hypoxia will be biphasic in that one initially will see hyperventilation followed by depressed ventilation. Third, in the infant respiratory rate can be decreased by afferent impulses from the upper airway. And fourth, the coordination between the postcricoarytenoid muscle responsible for opening the glottis and the diaphragm muscle is not developed fully, resulting in episodes where the airway is not opening to allow entrance of air with contraction of the diaphragm. Therefore, the child will be trylng to breathe against a closed glottis. The result of this is that neonates are likely to have irregular respiratory rates compared with the adult, and brief apneas in this age group are very common. Over the first few months of life this becomes less and less of a problem as the child develops. There are also simple anatomic problems or differences between the airway of the neonate and that of the older child or adult. The airway lumen itself is much smaller. The respiratory rate is also much higher. Neonates are said to be obligate nose breathers, and although one finds this is true in most instances, there are times when one finds children with bilateral choanal atresia who are able to survive initially until this diagnosis is made and treatment is started. There are also variations in the sleep/wake pattern in that infants frequently do not have a set pattern and it may take some time for a circadian rhythm to develop. Lastly, there are differences in basic respiratory physiology between the infant and the adult. In children who suffer from obstructive sleep apnea syndrome, there are some common features shared with the adult as far as the nature of the obstruction and its ability to be measured, and also some of the anatomic features. There is a significant difference in the symptomatology that the patient may suffer as a child, however, as well as significant differences in the treatments available and methods of diagnosis. In children, as with neonates, some central apneas may be found and may be perfectly normal. These periods would be considered abnormal, however, if on polysomnogram they were found to cause bradycardia or significant oxygen desaturations. This would be indicative of an inborn disorder of respiratory control that would require treatment. CAUSES OF OBSTRUCTIVE SLEEP DISORDERED BREATHING
There are many causes of obstructive sleep disordered breathing found in the pediatric age group that may not be found in the adult age
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group (Table 1).As in adults, obstructive apnea more commonly occurs because of upper airway obstruction; there may be significant lower airway compromise, however, because of vascular rings, tracheal webs, atresias, and goiter. The primary goal in treating these children is first to find out what the cause is and from there determine appropriate therapy. Sleep disordered breathing in children, as with adults, can be due to central Table 1. SOME OF THE CAUSES OF OBSTRUCTIVE SLEEP DISORDERED BREATHING IN INFANTS AND CHILDREN Anatomic
Upper airway Deviated septum Nasal polyps Enlarged turbinates Choanal stenosis or atresia Macroglossia Hypertrophy of tonsils and adenoids Micrognathia Epignathia Temporomandibular joint ankylosis Lower airway Laryngeal and tracheal webs Tracheal atresia Intrinsic tracheal lesions Extrinsic compression (goiter) Laryngotracheomalacia Congenital
Apert‘s syndrome Cri du chat syndrome Crouzon syndrome Down syndrome Nager’s syndrome Pierre Robin syndrome Prader-Willi syndrome Treacher Collins syndrome Cystic fibrosis Mucopolysaccharidoses (Hunter’s and Hurler’s syndromes) Juvenile rheumatoid arthritis Cerebral palsy Chiari malformation Cranial basal malformations Craniofacial microsomia Pharvngeal encephalocele Other
Myopathy Neuromuscular disease Neoplasm Familial factors Gastroesophageal reflux
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or obstructive phenomena or a combination of the two. Brief periods of central apnea can be common in infants and frequently are seen in children. This sometimes is referred to as idiopathic apnea or apnea of prematurity or apnea of infancy, depending on whether the child is premature or term. Before making this diagnosis, however, one must rule out infection, obstruction, seizure disorders, or other metabolic problems as a cause for a central apnea. Congenital central alveolar hypoventilation, otherwise known as Ondine's curse, may show long periods of central apnea." This disorder, if undiagnosed, has a very high mortality rate and even when diagnosed, may prove very difficult to control. Treatment usually requires some type of ventilatory assistance for the patient and various devices have been used successfully for this. Obstructive sleep apnea may be caused by the same disproportionate anatomy as found in adults. In addition to this, it also may be because of impaired coordination of the muscles in the respiratory tract, especially between the diaphragm and dilators of the respiratory tract, and also because of congenital anomalies, both anatomic and neurologic. Some of these anomalies may be immediately life-threatening in the neonate and require prompt treatment as a life-saving measure. In the first few days of life to 6 weeks of age, upper respiratory infections are the most common causes of obstructive apnea. This is because of a combination of copious secretions and small airway diameter and inability to clear the secretion. In older infants and children, large adenoids and tonsils are the most common reason for obstructive sleep apnea. This may be seen in relation to mucopolysaccharidoses or sickle cell disease.I7 Although obstructive apnea in children is generally a peripheral disturbance, it also may reflect a central brainstem dysfunction.' This may cause hypotonia to severe spasticity, including the muscles of the airway such as the tongue and vocal cords. Abnormal posturing and poor head control may obstruct the airway, as will poor swallowing, which would allow for sigruhcant buildup of secretion. When surgical treatment such as adenotonsillectomyis performed on these patients, one may see a transient worsening of these conditions because of the tendency to increase pooling because of decreased swallowing from pain and the effects of analgesic medications on the patient. Obstructions also may be complete or incomplete as in adults, and children with these problems may do much better when awake and worse with sleep and muscle relaxation. This may lead to significant changes during rapid eye movement (REM) sleep when there are maximal degrees of atonia. Obesity would appear to be a less frequent cause of airway obstruction in children, and this will be discussed later in the article.
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SYMPTOMS, SIGNS, AND THE EFFECTS OF SLEEP APNEA ON CHILDREN
In infants, apnea may manifest itself with metabolic alkalosis, and repeated episodes of severe apnea actually may cause asphyxia1 brain damage. Obstructive apnea and central apnea have been implicated as possible etiologies for sudden infant death syndrome (SIDS). In children the blood chemistries actually may show a metabolic acidosis, and repeated episodes of apnea may result in developmental delay^.^ One of the major differences between the adult apneic patient and the child is with weight. Whereas in the adult obesity is a common finding in sleep apnea, in children 27% will show failure to thrive. In those with a normal weight range, one third of the children will have some type of underlying facial deformity or neuromuscular disorder. It is felt that the inability to gain weight is due to several reasons. First are the changes that occur in a child’s behavior secondary to the disturbed sleep. Second, because of adenoid enlargement there usually is a decreased sense of smell, and eating is not particularly enjoyable to the patient; therefore, he or she tends not to eat as much. Also, it is very difficult for the child to swallow when the upper airway is significantly obstructed by the mass of the tonsils and adenoids. The child is unable to eat and breathe at the same time. Often their food preference is to very soft foods or liquids. It takes them quite a long time to get a meal down, sometimes longer than the parents are willing to give them. They also gag and choke easily and food will tend to stick in their throat, making adequate nutrition very difficult for these children. One also may see polycythemia in these children as in adults, along with systemic hypertension that may lead eventually to cor pulmonale. It is estimated that cor pulmonale is present in 25%of children with obstructive sleep apnea ~yndrome.~ During the daytime these children are frequently irritable, aggressive, hyperactive, and are discipline problems. Many children who have been placed on methylphenidate HC1 and are diagnosed as having hyperactivity or attention deficit disorders in fact suffer from sleep disorders. Many of these children will complain of early morning headache due to carbon dioxide retention. Their memory frequently is impaired, as is their concentration, and school performance subsequently will suffer because of this. Their behavior also may cause significant interferencewith a normal family life. In teenagers, excessive daytime sleepiness may lead to significant hypersomnolenceand motor vehicle accidents while driving. At nighttime, these children have significant snoring in almost 100% of cases, interrupted by periods of silence. They are very restless sleepers and tend to sleepwalk at night. Their sleep frequently is disturbed by bad
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dreams and nightmares. They tend to sleep with their head extended in order to open the pharyngeal airway as much as possible. Because of their hyperactivity during sleep, they frequently are diaphoretic, as well. Enuresis also may be a problem in these children; care must be made, however, in assigning this symptom to the child, and attention must be paid to his or her age and what is considered normal onset of bladder control at night. On examination the various congenital anomalies that have been found to be causative factors may be apparent readily to the physician. In addition, one may notice some hyponasal speech. As patients get older, they may develop adenoid facies or elongation of the midface from mouth breathing, as well as an open bite deformity as a result of their chronic attempt to adjust their airway to circumvent the obstruction. They also may develop a pectus excavatum as a result of chronically breathing against resistance at night. This may be aggravated in cases of partial daytime obstruction, as well. Some children will be frankly pickwickian, which will be notable in the waiting room or examination room. TESTING
As in adults with obstructive sleep disorders, testing is essential to making the diagnosis. The predictive value of a good history and physical examination by a physician familiar with sleep disorders in comparison to diagnosis made on polysomnogram is between 30% to 50%.23Of significance is that frequently adenotonsillectomyis performed based solely upon the symptomatology described by an observer and physical examination, and no testing is done on the patient. This would lead one to conclude that there may be a considerable number of adenotonsillectomies being performed for upper airway obstruction and sleep apnea that need not be done. In the same study, it was found that the symptoms with the highest predictive value were enuresis at 46% and snoring intensity of greater than 30 dB with a value of 60%. One of the major problems with polysomnography in children is that there is no well-defined demarcation between what is considered a normal and abnormal polysomnogram in this age group. One study states that the polysomnogram (PSG) is abnormal if the respiratory disturbance index is greater than 5.1° Another study has abnormal parameters of a respiratory disturbance index (RDI) of greater than 15 per hour, or 25 per hour for 1 hour.9 And yet another study defines an abnormal polysomnogram as an RDI greater than 1,0, saturations dropping below 92%, end tidal CO, of greater than 53 mm Hg, and hypoventilation duration greater than 60%.16
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Sleep somnography or recording of the snoring while the patient is asleep has been correlated with polysomnogram and does seem to have some predictive value as to the degree of apnea in patients with enlarged tonsils and adenoid^.'^ This technology is not able to differentiateobstructive apneas from central apneas, however. Endoscopy is also a useful tool in an attempt to determine sites of obstruction and to visualize what type of obstruction one may be dealing with, bearing in mind that congenital abnormalities or masses within the airway such as encephaloceles, laryngoceles, and so forth, although rare, may be a more common finding in children than in adults. Cephalometricradiographs and other imaging techniques are important to look at soft tissue anatomy, bony anatomy, and airway space. These are particularly important if surgical intervention, especially to the skeletal structures, is to be contemplated. Chest radiographs also may reveal an enlarged heart as a sign of chronic upper airway obstruction. Other tests also may provide useful pieces of information.Hematocrit may reveal polycythemia, arterial blood gases may reveal hypoxemia or hypercarbia, electrocardiograms (ECGs) and echocardiograms are useful to evaluate the heart, looking for possible right heart strain, and pulmonary function tests sometimes may show a saw-toothed pattern on flow volume loops, frequently seen with upper airway obstruction.
TREATMENT
The basic philosophy for treatment in the pediatric age group is to (1) eliminate or control the etiology of the obstructive breathing and (2) prevent episodes of serious breathing problems and their frequencyin order to decrease the risk of sequelae to repeated episodes of apnea. Treatment modalities can be divided into behavioral, medical, use of appliances, and surgery. Typical behavioral modifications are to decrease weight and try to improve sleep hygiene in the older child. In the neonate and infant, one tries to establish a regular sleep schedule. In addition, the physician should take a careful history of medication and drug use. In many patients, medications that have a sedative side effect may be used. Typical in younger children would be over-the-counter cold preparations being given before bedtime. In the older pediatric patient, one must consider drug use and alcohol use that may be causing aggravation of apnea. These histories sometimes may be very difficult to elicit, especially in the presence of a parent. Medical treatment may be used to treat factors aggravating or causing apnea or attempting to treat the apnea itself. Medical treatment of allergies
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and rhinitis is important, especially in the younger children with a smaller airway; one should avoid sedating antihistamines,however. Gastroesophageal (GE) reflux has the ability to increase the severity and number of apneas in a patient, and this should also be brought under control. If there is a question of reflux being present, appropriate diagnostic testing may need to be part of the work-up for the sleep disorder. There are medications that have been tried to control obstructive breathing disorders at night. Respiratory stimulants have not seemed to work very well. Protriptyline has been helpful in a few cases, but has not had consistent There are various devices available that will help control the apnea or alert the parent to significant apnea episodes. Continuous positive airway pressure (CPAP)long has been known to be an effective control measure for apnea in adults and is effective equally in children. In adults, the biggest problem has been with compliance with the use of the machine. In children, however, this is not as problematic as there is frequently parental supervision to ensure that the patient is compliant with the use of the apparatus. Dental appliances also have been used. Again, they do have a place in the treatment of the pediatric patient, especially in the course of treating patients with skeletal or dental problems contributing to the obstructive phenomena. Monitors are also useful in detecting significant apneas. Cardiorespiratory monitors are the most common type used and are more useful for central apnea than for obstructive sleep apnea. They should not be considered always as treatment devices. Pulse oximeters also fall into this category. Again, they basically are alerting and recording devices rather than actual treatment devices. Surgery has been the most common form of treatment in the pediatric age group and probably the most successfulform of treatment for obstructive breathing disorders for this patient population. Nasal surgery is necessary in some patients and the type of surgery depends upon what manner of obstruction one is dealing with. Septoplasty for deviated septums has been useful; because of concern for disruption of growth centers, however, a more conservative approach is taken in the younger age group than would be taken in adults. This procedure has been useful especially in children with a cleft lip or palate that frequently will have nasal obstruction on the side of the cleft. Nasal polyps can occur in the pediatric age group and may have to be removed in order to provide adequate airway. This commonly is needed in patients with cystic fibrosis. The nostrils may be narrow congenitally, and widening of the nostrils may have to be undertaken or even reconstruction of a nostril is needed in some craniofacial anomalies. Turbinates can become hypertrophied in allergy patients and the sue may need to be reduced. In the nasopharynx, one may have to correct a choanal atresia or choanal ste-
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nosis. One always must bear in mind that a nasal mass or nasopharyngeal mass may be originating from the central nervous system and an appropriate work-up should be taken prior to such excision. Adenotonsillectomy is the most common procedure performed in the pediatric age group for obstructive breathing disorders during sleep. It has been found to be effective 90% of the time when there is absence of craniofacial or neurologic abnormality.IO Even in cases of severe apnea where cox pulmonale may be present, there is usually prompt resolution of the symptomatology in the postoperative periodJ2 When treating the patient with adenotonsillectomy certain precautions must be taken that normally would not be taken in treating a patient with adenotonsillectomy for infectious etiology. Remembering the effects of the anesthetic and analgesic, there is the potential for temporary worsening of the symptoms in the immediate postoperative period and the airway must be monitored closely for this reason. Therefore, these procedures should not be done on an outpatient basis, but rather at least with an overnight stay and, in more severe cases, observation in an intensive care unit or stepdown setting. The patient should never be extubated until fully awake and able to guard the airway. Frequently, a nasopharyngeal airway is a useful adjunct in the recovery period. In some patients with significant hypopharyngeal airway compromise, an anterior tongue stitch is useful. One also should bear in mind that a patient may have more than one sleep disturbance and the physician should not develop a false sense of security that the patient has been cured by the adenotonsillectomy. Hypersomnolence, narcolepsy, or central apnea may exist still after the surgery and it is important that follow-up studies are performed to ensure that the sleep disorder has been treated adequately. It is especially true if there has not been adequate resolution of the symptoms. In some children with cleft palate, it has been shown that velopharyngeal flaps that have been used to treat velopharyngeal insufficiency may cause significant obstruction to the airway during ~1eep.I~ In these situations these flaps may need to be revised, or when the patient is older, if possible, completely taken down. Uvulopalatopharyngoplasty is performed in the pediatric age group, but not with the frequency that it is performed in the adult age group. Generally when it is performed, it is done in a more conservative fashion, especially with regard to resection of the midportion of the palate. If this procedure is done in conjunction with adenotonsillectomy, extreme caution must be taken as it has been shown that adenoidectomy performed in conjunction with a uvulopalatopharyngoplasty is one of the risk factors for development of significant nasopharyngeal inlet stenosis in the postoperative period.I4 Glossopexy also has been used in neonates and in patients with Pierre Robin syndrome. PSG indications have been devised by Freed et a17for this procedure. It is a reversible procedure when the airway has been
stabilized. In older patients requiring this procedure, the lower incisors may need to be removed in order to prevent breakdown of the site. Tracheotomy also is used in the pediatric age group. It probably is used more commonly in neonates and infants than in older children. As with adults, it does work quite well. Besides the usual problems seen with adults, however, there also are problems seen with its effects on language development and, in the older child, the psychosocial problems that arise from having a tracheostomy." Skeletal surgery, apart from that performed to correct congenital skeletal malformations, also is useful in carefully selected patients. By age 4, craniofacial growth is usually 60% of adult size and continues on to approximately age 16 in females and age 19 in males. When considering this type of surgery, one must try and determine whether the child will get better as he or she gets older and the facial bones grow in order to determine how aggressive one must be. There is some reluctance to do genioglossus advancements and hyoid myotomies, as well as bimaxillary advancement surgery in this age group, because of its potential effects on bone growth centers. Skeletal expansion surgery, however, has been shown to be quite useful in combination with soft tissue surgery in treating patients with craniofacial deformities? As mentioned, postoperative patients being treated for obstructive breathing disorders should be monitored closely. This is true especially in the younger patient, those with increased numbers of obstructive events on polysomnogram, patients in the lower percentile for weight and age, and those with abnormalities on their ECGs or echocardiograms.18Approximately 23% of patients that were treated surgically for obstructive sleep apnea had intermittent or continuous desaturations down to 70% or less in the immediate postoperative period. One also should remember that the effect of anesthetics and analgesics will increase airway collapse, and pediatric patients tend to have a decreased ventilatory response to elevated carbon dioxide 1e~els.I~ It also has been shown that postoperative pulmonary edema may ensue after relief of upper airway obstruction,and this can occur up to 12 to 14 hours postoperatively.8 In considering patients for surgical correction of their apnea, especially for adenotonsillectomy, one also should consider the degree of apnea. Patients with mild obstructive sleep apnea syndrome may get better spontaneously with age as the tonsils and adenoids regress in size normally. The treating physician also should make sure that the parents understand that the pathophysiology of obstructive sleep apnea in the child may be quite different from that in the adult, and that although adenotonsillectomy or other surgical interventions may cure the apnea in the child, there is a chance that as the patient gets older, apnea may reappear for different reasons.
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CONCLUSlON Although there are significant similarities in the process of obstructive breathing disorders in sleep in the pediatric age group in comparison to the adult age group, there also are some very significant differences. One must, therefore, take this into consideration when treating these patients, especially the smaller children, as these small airways are not terribly forgiving of errors in management. References 1. Arnold J, Allphin A. Sleep apnea in the neurologically impaired child. Ear Nose Throat J 7280-81,1993 2. Bonow M, St. John W, Bledsoe T Differential elevation by protriptyline and depression by diazepam of upper airway respiratory motor activity. Am Rev Respir Dis 1314-45, 1985 3. Brooks L: Treatment of otherwise normal children with obstructive sleep apnea. Ear Nose Throat J 72:77-79,1993 4. Brouillette R, Fernbach S, Hunt C: Obstructive sleep apnea in infants and children. J Pediatr 10031-40,1982 5. Brownell L, West P, Sweatman I, et al: Protriptyline in obstructive sleep apnea. N Engl J Med 307:1037-1042,1982 6. Cohen X, Ross D, Burstein F, et al: Skeletal expansion combined with soft tissue reduction in the treatment of obstructive sleep apnea in children: Physiologic results. Otolaryngol Head Neck Surg 119476-485,1998 7. Freed G, Pearlman M, Brown A, et a 1 Polysomnographic indications for surgical intervention in Pierre Robin’s sequence: Acute airway management and follow up studies after repair and take down of tongue-lip adhesion. Cleft Palate Craniofac J 25:151-155, 1988 8. Galvis A, Stool S, Bluestone C: Pulmonary edema following relief of acute upper airway obstruction. Arch Otolaryngol Head Neck Surg 80:112-128, 1980 9. Goldstein N, Sculerati N, Walsleben J, et a 1 Clinical diagnosis of pediatric obstructive sleep apnea validated by poIysomnogram. Otolaryngol Head Neck Surg 111:611-617, 1994 10. Guilleminault C, Korobkin R, Winkle R A review of 50 children with obstructive sleep apnea syndrome. Lung 159:275-287,1981 11. Guilleminault C, McQuitty J, Ariagno R, et a 1 Six infants with congenital alveolar hypoventilation syndrome. Pediatrics 70:684-697,1982 12. Hill W Some causes of backwardness and stupidity in children and the relief of these symptoms in some instances by nasophaqmgeal scarification. BMJ 2:711-712, 1889 13. Ingram R, Bishop J: Ventilatory response to carbon dioxide after removal of chronic airway obstruction. Am Rev Respir Dis 102:645-647, 1970 14. Katsantonis G, Friedman W, Krebs F, et al: Nasopharyngeal complications following uwlopalatopharyngoplasty. Laryngoscope 97:309-314,1987 15. Kravath R, Pollock C, Borowiecki B, et al: Obstructive sleep apnea and death associated with surgical correction of velopharyngeal insufficiency. J Pediatr 96:645-648, 1980 16. Marcus C, Carroll J, Coerne X, et al: Determinance of growth in children with obstructive sleep apnea syndrome. J Pediatr 125:556-562, 1994 17. Maddern B, Reed H, Ohen E, et al: Obstructive sleep apnea syndrome in sickle cell disease. Ann Otol Rhino1 Laryngol98:174-178,1989 18. McColley S, April M, Carroll J, et a1 Respiratory compromise after adenotonsillectomy in children with obstructive sleep apnea. Arch Otolaryngol Head Neck Surg 118:940943,1992
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19. Potsic W Comparison of polysomnogram and sonography for assessing regularity of respiration during sleep in adenotonsillar hypertrophy. Laryngoscope 971430-1437, 1987 20. Roloff D, Aldrich M: Sleep disorders and airway obstruction in newborns and infants in sleep apnea. Otolaryngol Clin North Am 23:639-650, 1990 21. Singer L, Kercsmar C, Legies G, et al: Developmental sequelae of long-term infant tracheostomy. Dev Med Child Neurol31:224-230,1989 22. Sofer S, Weinhouse E, Tal A, et al: Cor pulmonale due to adenoidal and tonsillar hypertrophy or both in children. Chest 93:119-122, 1988 23. Wang R, Elkins T, Keech D, et al: Accuracy of clinical evaluation in pediatric obstructive sleep apnea. Otolaryngol Head Neck Surg 118:69-73,1998 Address reprints requests to Jack Coleman, MD Nashville Ear, Nose and Throat Clinic Atrium Building Suite 200 250 25th Avenue North Nashville, TN 37203-1632