Sleep-Related Obstructive Disordered Breathing in Cleft Palate Patients after Palatoplasty Edmund Rose, M.D., D.D.M., Richard Staats, M.D., Ulrike Thissen, D.D.M., Jörg-Eland Otten, Ph.D., M.D., D.D.M., Rainer Schmelzeisen, Ph.D, M.D., D.D.M., and Irmtrud Jonas, Ph.D., D.D.M. Freiburg, Germany

Sleep-disordered breathing is frequently associated with children presenting congenital midface defects. Because of structural and functional anomalies in the upper airway, children with cleft palate, especially after surgery, may carry a higher risk of developing sleep-disordered breathing. However, the presence of such sleep-disordered breathing in older cleft palate children has not been emphasized. The aim of this comparative overnight cardiorespiratory sleep study was to evaluate cleft palate patients according to sleep-disordered breathing. A group of 43 cleft palate children (17 girls and 26 boys; mean age, 12.1 ⫾ 3.8 years) was compared with a control group of 20 randomly selected, noncleft children matched for age, sex, and body mass index. None of the patients suffered from manifest sleep-disordered breathing. Cleft palate patients had a statistically significantly higher respiratory disturbance index and snoring index, but no increased apnea index. The data suggest that cleft palate patients having undergone primary closure of the palate demonstrate microsymptoms of nocturnal upper airway obstruction. (Plast. Reconstr. Surg. 110: 392, 2002.)

at higher risk of developing obstruction events during sleep.3,4 In childhood, the clinical presentation of sleep-disordered breathing differs significantly from adult sleep-disordered breathing5,6; it is considered a serious problem and an important cause of childhood morbidity. In sleepdisordered breathing, episodes of upper airway obstruction are usually associated with loud snoring, arousals, sleep fragmentation, intermittent hypoxemia and hypercapnia, and nocturnal hypertension. In children, daytime sleepiness may occur, but concentration difficulties and problems in school are seen more often. The long-term consequences of sleepdisordered breathing may include sustained daytime hypertension, and increased cardiorespiratory and cerebrovascular morbidity, growth and development disturbances, neurobehavioral problems, and mortality. Not all symptoms are clinically present, especially in mild cases; thus, sleep-disordered breathing often goes unrecognized in children. Although the risk of developing upper airway obstruction after palatoplasty is considered very slight,7 there are recent reports of an increased incidence of sleep-disordered breathing in patients secondary to palatoplasty8; however, the knowledge of this disorder remains limited in this population. Parents of cleft palate patients often report their children’s snoring and noisy breathing during sleep, and these clinical find-

Sleep-disordered breathing in adults is clinically associated with the occurrence of repetitive episodes of complete or partial obstruction of the upper airway, disrupting normal ventilation during sleep. In addition to other risk factors such as obesity and upper and lower respiratory tract problems, hypertrophy of the adenoids and tonsils is considered the most common cause of sleep-disordered breathing in infants.1,2 Children with craniofacial syndromes and malformations such as micrognathia and maxillary hypoplasia that involve anatomic or functional narrowing of the airway are

From the Department of Orthodontics and Department of Maxillofacial Surgery, School of Dental Medicine, and Department of Pneumology, Robert Koch Clinic, Medical School, University of Freiburg. Received for publication July 18, 2001; revised November 14, 2001. Preliminary results were presented at the 9th International Congress on Cleft Palate and Related Craniofacial Anomalies, in Göteborg, Sweden, on June 25, 2001.

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ings are considered initial symptoms for sleepdisordered breathing in children. The aim of this investigation was to assess patients of the School of Dental Medicine, University of Freiburg in Breisgau with repaired cleft palate by means of a sleep study examining sleepdisordered breathing. PATIENTS

AND

METHODS

Study Group

We examined 63 subjects between the ages of 6.3 and 22.5 years between June of 1999 and April of 2000 with overnight polygraphic studies. The study group included 43 subjects (17 girls and 26 boys; mean age, 12.1 ⫾ 3.8 years; mean body mass index, 17.5 ⫾ 2.9 kg/m2) with no other medical conditions apart from a repaired unilateral or bilateral closure of the cleft palate. According to our treatment sequence, all infants had had their clefts repaired at the mean age of 13.0 ⫾ 4.1 months (range, 8 to 21 months) using a modified Langenbeck, Ernst, Veau, and Axhausen technique, described previously by Delaire.9 All patients routinely visited the cleft palate clinic at the University of Freiburg. The patients’ different cleft types are listed in Table I. Seven of them had undergone a velopharyngoplasty according to Sanvenero-Rosselli at the age of 10.3 ⫾ 3.1 years (range, 6 to 14 years). Because of a lack of normal sleep parameters in this age group, we examined a control sample of 20 asymptomatic, age-, sex-, and weightmatched noncleft subjects (eight girls and 12 boys; mean age, 12.1 ⫾ 2.7 years; mean body mass index, 17.8 ⫾ 2.6 kg/m2). The control subjects were randomly selected patients from the department of orthodontics. They had no craniofacial syndromes; were nose breathers; and had no history of ear, nose, and throat problems. Patients with the following criteria were excluded from the study: those with prior treatment of sleep-disordered breathing, including TABLE I Number of Subjects According to Cleft Type

Cleft Type

Female

Male

Total

UCLP BCLP CP

3 12 6

9 4 9

12 16 15

UCLP, unilateral cleft lip and palate; BCLP, bilateral cleft lip and palate; CP, cleft palate.

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tonsillectomy, adenoidectomy, recurrent tonsillitis, frequent colds (six or more per year), dysphagia, and continuous positive airway pressure therapy; or all forms of syndromic clefting, including Pierre Robin sequence, Goldenhar sequence, and trisomy 21. Before the study, the subjects’ parents were informed of the investigation and consented to the study protocol. The collection of anamnestic details and clinical examination, including assessing tonsil size,10 was carried out on all subjects. Many of the sleep-disordered breathing–specific data, including noisy breathing, snoring, mouth breathing during sleep, bruxism, nocturnal awakenings, sweating during sleep, morning headache, daytime sleepiness, recurrent upper airway infections, and enuresis, were obtained from a standardized questionnaire and completed by discussion with both patients and parents. Polygraphy

Standard overnight cardiorespiratory monitoring was accomplished with a portable multichannel computerized system (Merlin, Heinen⫹Löwenstein, Bad Ems, Germany) equipped with special pediatric sensors at the subjects’ homes. The subjects were visited at home by a physician who distributed and administered questionnaires, took physical measurements, and provided instructions on the use of the recording monitor. It consisted of oronasal airflow (thermistor), thoracic and abdominal wall motion (piezoelectric band), electrocardiography, finger pulse oximetry, heart rate, body motion sensor, and parapharyngeal sound measurement. Sleep was recorded for a minimum period of 6 hours; if the first registration was not completely monitored, a second sleep study was carried out the following night. The apnea index was defined as the number of obstructive and mixed apneas of at least two respiratory cycles’ duration per hour of sleep time. Hypopneas were defined as a qualitative reduction in thermistor airflow of more than 50 percent, associated with a desaturation of more than 4 percent. The respiratory disturbance index was defined as the number of apneas and hypopneas per hour of sleep. To assess the arterial oxygen saturation, the minimum and the mean partial pressure of arterial oxygen levels were determined. Oxygen saturation measurements associated with a poor pulse waveform were discounted. An oxygen desaturation below 92 percent was considered

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abnormal. The desaturation index was calculated as the number of desaturation episodes below 4 percent of the mean oxygen saturation per hour of sleep. The snoring index was defined as the number of snoring events lasting more than 10 seconds per hour of sleep. Data Analysis

Evaluation of the data was performed manually on the computer the following day by a single investigator trained in the field of somnology, and this was subsequently reviewed by the principal investigator (E.R.) to ensure consistency. Neither investigator was aware of the craniofacial diagnosis of the subject when evaluating the sleep protocol. Data were analyzed using the statistical program SAS 6.12 (SAS Institute, Inc., Cary, N.C.). Comparison between study and control subjects was carried out using a nonparametric signed rank test according to Kruskal-Wallis. A chi-square test was applied to test distribution differences between the anamnestic parameters from the questionnaire. If statistical significance was achieved, a logistic regression analysis was used to investigate differences between pairs of groups. Data were shown as mean ⫾ SD. The zero hypothesis was tested at a level of significance of p ⬍ 0.05, or p ⬍ 0.01.

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TABLE II Respiratory Parameters in the Sleep Study

Respiratory Parameters

Respiratory disturbance index (events/hr) Apnea index (events/hr) Mean oxygen saturation (%) Minimal oxygen saturation (%) Desaturation index (events/hr) Snoring index (events/hr)

CPP (n ⫽ 43) (Mean ⫾ SD)

NCC (n ⫽ 20) (Mean ⫾ SD)

p Value

2.44 ⫾ 1.29

0.8 ⫾ 0.53

⬍0.001

0.23 ⫾ 0.21 96.1 ⫾ 0.9 86.4 ⫾ 5.4 0.7 ⫾ 0.48 3.04 ⫾ 1.19

0.21 ⫾ 0.13 96.2 ⫾ 0.9 85.0 ⫾ 4.1 0.32 ⫾ 0.23 1.2 ⫾ 0.41

NS NS NS ⬍0.01 NS

CPP, cleft palate patient; NCC, noncleft control group; NS, not significant.

studies: snoring was found statistically more often in cleft patients than in the control group; and cleft palate patients had a significantly higher, although not pathologic, respiratory disturbance index than noncleft patients. This finding was mainly because of hypopneas rather than total obstructions, because there was no apnea index difference between the two groups. Although there were no differences in the mean and the minimal oxygen saturation, the number of desaturations, reflected by the desaturation index, was also statistically higher in the cleft palate patient group. Patients who had pharyngeal flap surgery showed no measurable differences from the patients without that procedure.

RESULTS

DISCUSSION

According to the anamnestic reports and the clinical assessment, there was no presumption of sleep-disordered breathing in any of the patients or subjects. There were no statistical differences among the size of the tonsils within both groups. In the nocturnal polygraphic recording, only two cleft patients were found with an apnea index above 5 events per hour, and these were mainly central and not obstructive events. None of the patients had an increased desaturation index. However, we did find statistical respiratory differences between both groups during sleep. The respiratory data are presented in Table II. None of the patients having undergone pharyngeal flap surgery had any sign of sleep-disordered breathing. Statistically, the parents of cleft palate patients reported more frequently the occurrence of arousals (p ⬍ 0.05), snoring (p ⬍ 0.01), openmouth breathing (p ⬍ 0.001), and sleep fragmentation (p ⬍ 0.01) than was the case regarding patients in the noncleft reference group. These data were objectified by the overnight

Although we found minor elevated respiratory parameters in patients with cleft repair, we could not find any patients with manifest sleepdisordered breathing in the group studied. This finding is in contrast to a recent report.8 Unfortunately, the authors did not mention therein the surgical procedure that had been used; therefore, a reason for the disparate results cannot be determined. Sleep-disordered breathing in children has recently received considerable attention. In the cleft population, sleep-disordered breathing is described in the following distinct populations: patients with craniofacial syndromes such as Pierre Robin sequence3; Goldenhar sequence11; trisomy 2112; Treacher-Collins syndrome13; and patients with cleft palate who have undergone secondary “speech-corrective” surgery, including the placement of a pharyngeal flap, or treatment with a sphincter pharyngoplasty, who have a higher incidence of obstructive symptoms. 4,11,14 –17 Because of structural and functional abnormalities, the pa-

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tency of the upper airway’s surrounding tissue is reduced during sleep and may fall backward, causing obstruction of the pharyngeal passage, resulting in periods of hypoventilation, apnea, and snoring. Adult definitions and criteria do not directly apply to children, and two to five apnea events per hour of sleep are considered abnormal in children. The typical symptoms of sleepdisordered breathing are noisy and labored breathing, snoring, and morning headache; symptoms that characterize adult sleep-disordered breathing, such as excessive daytime sleepiness and hypomobility, are uncommon in children. Unrecognized sleep-disordered breathing can lead to pulmonary hypertension, growth failure, systemic hypertension, cor pulmonale, and neurocognitive abnormalities.18 In our study, snoring, mouth-breathing, and sleep fragmentation were reported significantly more often than in the control study by the respective parents. This observation of extra snoring in these patients does not reflect severe desaturation events. At present, it is not known whether these findings should be assessed as clinically irrelevant, as perhaps a distinct symptom during growth, or as precursors of adult obstructive sleep apnea with all the subsequent symptoms. Furthermore, it remains speculative as to whether sleep-disordered breathing plays a role in the growth deficiency observed in clefted children.19,20 Several parameters may contribute to the lack of airway patency during sleep, such as maxillary hypoplasia, reduced upper airway neuromotor and muscular tone, adenotonsillar hypertrophy, and surgery in the palate and the velopharyngeal region. Most children suffering from sleep-disordered breathing show improvement following tonsillectomy and adenoidectomy.1,21,22 In cleft palate patients, those procedures may affect velopharyngeal competence and initiate a rhinophonia aperta. Therefore, the decision to correct underlying anatomic abnormalities in cleft palate patients with snoring and/or mild sleep-disordered breathing must be made with great caution. Data exist suggesting that sleep-disordered breathing in children is not caused by structural abnormalities alone, but also by dynamic, neuromuscular factors.23 Furthermore, it is unknown whether microsymptoms of sleepdisordered breathing persist in adults or whether they self-correct because of structural

changes within the upper airway, like the change in orientation of the pharynx, with growth from the more horizontal to the more vertical type, and the natural involution of the adenoid pad.24 The development of obstructive events during sleep may be affected by the type of surgical technique used; however, this study was not designed to favor a certain surgical procedure or treatment sequence. Moreover, the intent of our investigation was to screen cleft palate patients according to sleep-disordered breathing. Furthermore, this study provides no information on the acute postoperative respiratory situation of the patients. That might be totally different, for several reasons, including postoperative edema. Sleep-disordered breathing significantly affects sleep architecture in children, with a decrease primarily in slow-wave sleep. Clinically, parents of the cleft palate patient group reported more frequent nocturnal awakenings. One of the shortcomings of this study was that we carried out cardiorespiratory polygraphy at home, without recording sleep stages. Complete polysomnographic measurements in a sleep laboratory with mean and maximum endtidal carbon dioxide registration provide more precise data in children with congenital midface defects, and these should be performed in a subsequent prospective and longitudinal study. CONCLUSIONS

There was no increase in the incidence of manifest obstructive sleep apnea on our repaired cleft palate patients, but there were more frequent hypopneas and snoring, a factor not reflecting severe desaturation events and probably not affecting daytime behavior of these patients. Nevertheless, the clinician dealing with such patients should be aware of sleep-disordered breathing, as an increased hypopnea and snoring index represents microsymptoms that may develop into more serious problems. We conclude from this study that in cases where parents report a child’s frequent snoring, a somnography screening investigation is helpful in documenting and clarifying the degree of the disorder. Patients should, therefore, be reexamined at a later developmental stage.

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Edmund C. Rose, M.D., D.D.M. Department of Orthodontics School of Dental Medicine Albert-Ludwigs University of Freiburg Hugstetter Strasse 55 79106 Freiburg i. Br. Germany [email protected]

10.

11.

12.

ACKNOWLEDGMENT The authors thank Prof. Dr. Jürgen Schulte-Mönting, Center for Biometrics and Medical Informatics, University of Freiburg i. Br., for his assistance with the statistical analyses. REFERENCES 1. Marcus, C. L. Clinical and pathophysiological aspects of obstructive sleep apnea in children. Pediatr. Pulmonol. Suppl. 16: 123, 1997. 2. Redline, S., Tishler, P. V., Schluchter, M., et al. Risk factors for sleep-disordered breathing in children: Associations with obesity, race, and respiratory problems. Am. J. Respir. Crit. Care Med. 159: 1527, 1999. 3. Abramson, D. L., Marrinan, E. M., and Mulliken, J. B. Robin sequence: Obstructive sleep apnea following pharyngeal flap. Cleft Palate Craniofac. J. 34: 256, 1997. 4. Hochban, W., and Hoch, B. Obstruktive Schlafapnoe bei Kindern: Eine interdisziplinäres Behandlungskonzept mit besonderer Berücksichtigung kraniofaziale Veränderungen. Pneumologie 52: 147, 1998. 5. Standards and indications for cardiopulmonary sleep studies in children: American Thoracic Society. Am. J. Respir. Crit. Care Med. 153: 866, 1996. 6. Marcus, C. L. Obstructive sleep apnea syndrome: Differences between children and adults. Sleep 23 (Suppl. 4): S140, 2000. 7. Orr, W. C., Levine, N. S., and Buchanan, R. T. Effect of cleft palate repair and pharyngeal flap surgery on upper airway obstruction during sleep. Plast. Reconstr. Surg. 80: 226, 1987. 8. Paditz, E., Leniewsky, G., Kanitz, G., et al. Obstruktive Schlafapnoe-Syndrome (OSAS) bei Kindern und Jugendlichen mit operierter Lippen-Kiefer-Gaumenspalte (LKGS). Monatsschr. Kinderheilkd. 146: 149, 1998. 9. Delaire, J. Considerations sur la reconstitution de la

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