Prevalence and Severity of Obstructive Sleep Apnea and Snoring in Infants With Pierre Robin Sequence
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1 Prevalence and Severity of Obstructive Sleep Apnea and Snoring in Infants With Pierre Robin Sequence Iee Ching W. Anderson, M.D., Ahmad R. Sedaghat, M.D., Ph.D., Brian M. McGinley, M.D., Richard J. Redett, M.D., Emily F. Boss, M.D., Stacey L. Ishman, M.D., M.P.H. Objective: To evaluate the prevalence and severity of obstructive sleep apnea in infants with Pierre Robin sequence prior to airway intervention and determine whether snoring correlates with the presence of obstructive sleep apnea in this population. Design: Retrospective case series. Setting: Urban tertiary care teaching hospital. Participants/Methods: Review of infants with Pierre Robin sequence who underwent polysomnography in the first year of life from 2002 to Only results from the initial polysomnography were analyzed. A subgroup of consecutive prospectively tested patients was also evaluated. Results: A total of 33 infants with Pierre Robin sequence were identified. Of these, 13 (39%), 11 girls and two boys, underwent polysomnography in the first year of life. The mean age at evaluation was 48 days (range, 7 to 214 days). Seven nonconsecutive and six consecutive patients were included, and no significant differences were seen between groups. Obstructive sleep apnea was identified in 11 of 13 (85%) infants. The mean obstructive apnea-hypopnea index was 33.5 (range, 0 to 85.7). Obstructive sleep apnea severity was mild in 2 of 11 (18%), moderate in 3 of 11 (27%), and severe in 6 of 11 (55%). Mean endtidal PCO 2 measurements were elevated at 59 mm Hg (range, 47 to 76 mm Hg). Mean oxygen saturation nadir was decreased at 80% (range, 68% to 93%). Snoring occurred in only 7 of 13 (54%). Of the subjects with obstructive sleep apnea, snoring occurred in 6 of 11 (55%). Conclusion: The high incidence of obstructive sleep apnea in this group suggests that polysomnography should be promptly performed in children with Pierre Robin sequence. Although snoring was seen in the majority, the absence of snoring did not exclude the presence of obstructive sleep apnea. KEY WORDS: infants, OSA, Pierre Robin sequence, snoring First described by Parisian stomatologist Pierre Robin in 1923, the Pierre Robin sequence (PRS) refers to a constellation of congenital anomalies characterized by micrognathia and glossoptosis, with or without cleft palate (Robin, 1923, 1934). Pierre Robin sequence can be seen in isolation or can be associated with other congenital Dr. Anderson, Department of Otolaryngology, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, and Harvard Medical School, Boston, Massachusetts. Dr. Sedaghat, Department of Otolaryngology, Harvard Medical School, Boston, Massachusetts. Dr. McGinley, Department of Pediatrics, Eudowood Division of Pediatric Pulmonology; Dr. Redett, Department of Surgery, Division of Plastic Surgery; and Dr. Boss and Dr. Ishman, Department of Otolaryngology Head and Neck Surgery, Johns Hopkins School of Medicine, Baltimore, Maryland. Presented at the American Cleft Palate Craniofacial Association Annual Meeting, April 2009, Scottsdale, Arizona. Submitted May 2010; Accepted July Address correspondence to: Dr. Stacey L. Ishman, Department of Otolaryngology Head and Neck Surgery, Johns Hopkins School of Medicine, 601 North Caroline Street, Room 6231, Baltimore, MD sishman1@jhmi.edu. DOI: / anomalies or syndromes (Shprintzen, 1992). The inciting event is thought to be micrognathia with resultant glossoptosis, in which the tongue lies in a more posterior and superior position within the oropharynx. The retroposition of the tongue prevents the palatal shelves from coming together, leading to cleft palate formation (Breugem and Mink van der Molen, 2008). Airway obstruction is common in patients with PRS, likely secondary to the presence of micrognathia and glossoptosis. In addition, glossoptosis alone, with or without PRS, has been associated with obstructive sleep apnea (OSA) in children (Donnelly et al., 2000). However, the prevalence and severity of upper airway obstruction and OSA has not been well characterized in children with PRS. Management options for airway obstruction in children with PRS include prone positioning, nasopharyngeal airway placement, endotracheal intubation, tongue-lip adhesion, tracheostomy, and mandibular distraction. In one recent series, nonsurgical and surgical airway intervention beyond prone positioning was required in more than 50% of children with PRS due to airway obstruction 614
2 Anderson et al., OSA AND SNORING IN PIERRE ROBIN SEQUENCE 615 (Meyer et al., 2008). However, even when daytime airway obstruction is amenable to prone positioning alone, children with PRS are still at risk for OSA given the structural characteristics of their upper airways. Obstructive sleep apnea can be overtly manifest with noisy breathing, snoring, retractions, and gasping or choking episodes during sleep (Muzumdar and Arens, 2008). The presence of snoring, in particular, is commonly used as a clinical office screen for the possible presence of upper airway obstruction. The condition, however, is difficult to discern clinically, particularly in infants where apnea often occurs without clinically obvious obstructive symptoms (Singer and Sidotti, 1992). Even when a history of snoring is present, this symptom alone is unable to distinguish between primary snoring and sleep apnea (Carroll et al., 1995). Untreated OSA is associated with failure to thrive, cognitive and behavioral deficits, pulmonary hypertension, and congestive heart failure (Spicuzza et al., 2009). The purpose of this study was to evaluate the prevalence and severity of OSA prior to airway intervention in infants with PRS and to determine whether the subjective presence of snoring was associated with the presence of OSA in this population. Data Collection MATERIALS AND METHODS After approval by the Johns Hopkins School of Medicine Institutional Review Board, a case series study was performed to evaluate infants with PRS who received care at the Johns Hopkins Hospital from 2002 to Children were diagnosed with PRS if they had retrognathia, glossoptosis, and clinical signs of respiratory obstruction. Eleven of the 13 also had U-shaped clefts. Although the testing in the first seven patients reported was not collected in a systematic fashion, all the patients seen from January 1, 2006, until May 2007 were studied with polysomnography (PSG) and are represented as patients 8 through 13. Differences between these two groups were compared with a Student s t test. Polysomnography Standard overnight, 16-channel PSG was performed in the Johns Hopkins Pediatric Sleep Laboratory. The majority of sleep studies were performed with Somnologica (Embla, Broomfield, CO). Signals included electroencephalograms (leads C3-A2, C4-A1, and O1-A2), left and right electrooculograms, submental electromyogram, tibial electromyogram, electrocardiogram, and oxyhemoglobin saturation (Masimo, Irvine, CA). End-tidal CO 2 (Novametrix, Murrysville, PA) was acquired in all participants. Airflow was acquired with a nasal cannula (Salter Labs, Arvin, CA) connected to a differential pressure transducer (Pro-Tech, Mukilteo, WA). Respiratory effort was assessed with thoracic and abdominal inductive plethysmography (Embla), and body position was monitored via infrared video camera. Several studies were performed using Alice (Respironics, Murrysville, PA), which uses the signals above with the exception of the respiratory effort, which was assessed with a strain gauge with piezoelectric crystals. Snoring, when present, was graded on a subjective clinical scale of 1 (least) to 4(greatest) by the sleep technologist, based on duration and volume. Only results from the initial PSG, prior to surgical intervention, were analyzed. Results were interpreted by pediatric sleep medicine physicians at the Johns Hopkins Hospital. Analysis An apnea was defined as complete absence of airflow for at least two breath cycles. Apneas were identified as obstructive or central based on respiratory effort signals. A mixed apnea was identified by the absence of airflow associated with both the presence and absence of respiratory effort during the event. Obstructive and mixed apneas were grouped as obstructive for the purpose of analysis. A hypopnea was defined as a decrease in airflow of $50% for at least two breaths associated with a $3% decrease in oxygen desaturation or an electrocortical arousal from sleep (American Academy of Sleep Medicine [AASM], 2007). These polysomnographic event definitions are based upon the recommendations of the AASM. The respiratory disturbance index (RDI) was calculated as the number of respiratory events (apneas and hypopneas) divided by the total sleep time. The obstructive apnea-hypopnea index (OAHI) was calculated as the number of obstructive apneas and hypopneas divided by the total sleep time; central apneas were excluded from this calculated value. Standard research definitions for OSA severity were used, based on the OAHI value, with mild obstructive sleep apnea defined as 1 to.5 events per hour, moderate as 5 to,10 events/ hour and severe OSA defined as $10 events/hour (Katz and D Ambrosio, 2008). Central sleep apneas were not significant and were excluded from the analysis. Statistical Analysis Descriptive statistics were carried out to examine the distribution of measurement values. An unpaired t test with Welch correction was used to evaluate differences between groups for peak end-tidal CO 2 and oxygen saturation nadirs because they both had a normal distribution but nonequivalent standard deviation between groups. A nonparametric test, the Mann-Whitney U test, was used to evaluate differences between groups for OAHI because the nonconsecutive patient group was not normally distributed; p values of,.05 were used to determine significance throughout the analysis. Data were analyzed using Stata Statistical Software: Release 10.1 (Stata Corporation, College Station, TX).
3 616 Cleft Palate Craniofacial Journal, September 2011, Vol. 48 No. 5 TABLE 1 Demographic and Polysomnographic Data Study Subject Gender Age at PSG* (d) Snoring (Clinical Scale 0 to 4) OAHI OSA Severity OAI HI Peak End-Tidal CO 2 (mm Hg) O 2 Saturation Nadir (%) 1 F Mild F Severe F Severe M Moderate F Mild F Severe F None M Moderate F Severe F Moderate F Severe F None F Severe Mean (1 7) 86% F Mean (8 13) 83% F Overall mean 85% F * PSG 5 polysomnography; OAHI 5 obstructive apnea-hypopnea index; OAI 5 obstructive apnea index; HI 5 hypopnea index; d 5 days. RESULTS A total of 33 infants with PRS were identified. Thirteen infants (39%) underwent PSG in the first year of life prior to any surgical airway intervention. Eleven were girls (85%) and two were boys (15%). The mean age at evaluation was 48 days (range, 7 to 214 days) (Table 1). Although the first seven patients were nonconsecutive, the last six patients underwent consecutive PSG evaluation. Evaluation of the nonconsecutive and consecutive PSG groups revealed similar OAHI means of 30.5 versus 37 events per hour, respectively (p 5.63). In addition, the difference between groups for peak CO 2 values were nonsignificant, with a mean of 61.9 in nonconsecutive patients and 55.3 in consecutive patients (p 5.16). The difference in oxygen saturation nadir values was also nonsignificant, with a mean nadir of 82.6 in the nonconsecutive group and 77.5 in the consecutive group (p 5.24). In light of the similarities between groups, the remainder of the analysis was reported for overall totals. Obstructive sleep apnea was identified in 11 of 13 (85%). For those with OSA, the mean RDI was 40.4 (range, 3.3 to 85.7) and mean OAHI was 39.5 (range, 1.3 to 85.7). The severity of OSA ranged from mild disease in 2 of 11 (18%) to moderate disease in 3 of 11 (27%) and severe disease in 6 of 11 (55%) (Fig. 1). Obstructive apneas were seen in 11 of 11 (100%), and hypopneas were seen in 6 of 11 (55%). Obstructive apneas were 2.5 times more common than hypopneas (mean, 28.4 per hour versus 9.8 per hour). Central sleep apneas were infrequent, with a mean of 0.8 per hour (range, 0 to 4.1 per hour). Peak end-tidal PCO 2 measurements were elevated, with a mean of 59 mm Hg (range, 47 to 76 mm Hg). The mean oxygen saturation nadir in this group of patients was decreased, with a mean of 80% (range, 68% to 93%). Whereas the majority of study subjects had OSA, snoring was observed in only 7 of 13 (54%) of the infants. Of the children with OSA, only 6 of 11 (55%) snored, as did one of two (50%) of patients without OSA. Five of 11 (45%) subjects with OSA did not snore. Snoring did not appear to correlate with OSA severity. Neither of the subjects with mild OSA snored. Snoring was heard in three of three (100%) subjects with moderate OSA but only three of six (50%) subjects with severe OSA (Fig. 2). Evaluation of other symptoms seen in the children with PRS revealed that feeding problems, retractions, severe glossoptosis, and degree of retrognathia were inconsistently recorded. In addition, feeding often was not attempted due to respiratory concerns or not commented on in the medical record. Retrognathia was mentioned consistently, but degree of retrognathia was not consistently recorded. However, evaluation of the existing data reveals that five of the six infants without snoring were described as having mild retrognathia, with degree of retrognathia not com- FIGURE 1 Range of OSA severity: mild (AHI 1 to,5 events/hour), moderate (5 to,10 events/hour), or severe ($10 events/hour).
4 Anderson et al., OSA AND SNORING IN PIERRE ROBIN SEQUENCE 617 FIGURE 2 Snoring by OSA severity. mented on in the sixth. Whereas two of the patients with snoring were described as having mild retrognathia (5 to 7 mm), another was described as having moderate-severe, and two others had severe retrognathia (as much as 15 mm). The conditions of the last two patients in this category were not labeled. It is possible that there is a trend, given that patients with no snoring were more likely to be described as having mild retrognathia and those with snoring were more likely to be characterized as having moderate or severe. This has led to a change in our practice to more consistently record these variables in the future. DISCUSSION This preliminary study demonstrates a high prevalence (85%) of OSA in a small cohort of infants (age less than 1 year) with PRS who underwent PSG. In a subgroup of six consecutive patients, the prevalence of OSA was 83%. The majority of the infants (69%) had moderate or severe OSA. Snoring is an unreliable clinical indicator of airway obstruction during sleep, given that 50% of the study subjects with severe OSA did not demonstrate snoring. Evaluation of consecutive versus nonconsecutive patients revealed no significant differences in OAHI, saturation nadir, or peak end-tidal CO 2 values between groups, and therefore results were reported in aggregate. If it is assumed that all those without testing had no evidence of OSA, then the overall rate of OSA in PRS patients is 11 of 33 or 33%. Prior comparable studies of children with PRS have also found a high prevalence of OSA in this population. Gilhooly and colleagues (1993) studied 13 infants with PRS with PSG and found that 46% had significant airway obstruction. This study used four-channel sleep studies (electrocardiogram, respiratory motion, airflow, and oxygen saturation), which may account for the discrepancy in prevalence. A larger study by Bravo and colleagues (2005) looked at 52 children with PRS who had been referred to PSG for snoring or sleep-disordered breathing symptoms and found that 31 children, or 60%, had OSA by polysomnographic criteria. This report used an RDI of 5 to 20 events per hour, approximating the adult criteria for mild OSA, to identify sleep-disordered breathing in these children. Additionally, a stricter definition of hypopnea was used, requiring a decrease in airflow of at least 50% with $5% decrease in oxygen saturation. Of the children diagnosed with mild OSA, 25 would be reclassified as moderate to severe OSA in our evaluation. A retrospective review of 11 consecutive infants with PRS by Wilson et al. (2000) found that 10 of the 11, or 91%, had significant airway obstruction as measured by PSG; however, severity was not reported in this study. In addition, gas-exchange abnormalities were noted with decreased oxygen levels and elevated carbon dioxide levels. Although comparative values for these parameters have not been well studied in infants, normal carbon dioxide levels have been noted to be less than 50 mm Hg in a population study of 66 children aged 2 to 9 years (Traeger et al., 2005). In the same study, oxygen saturation levels were noted to be 97% 6 1%, with a nadir of 92% 6 3%. The absence of snoring in infants with PRS does not necessarily indicate that OSA is not present. Snoring was noted in 6 of 11 (55%) of the infants with OSA. However, 5 of 11 (45%) of infants with PRS who were found to have OSA did not snore, including three of six (50%) with severe OSA. This may be similar to the infants evaluated in the series by Wilson et al. (2000), in which six of seven (86%) infants with PRS were evaluated by PSG between 24 and 51 days of age due to failure to thrive. These children had no clinical airway symptoms and presumably no report of snoring; although, snoring itself was not specifically mentioned. Unfortunately, we did not collect snoring data on those patients not tested to provide some comparison to the group who underwent PSG testing. Diagnosis and treatment of OSA in the PRS patient population is of critical importance for several reasons. First, upper airway obstruction in infants with PRS may not be clinically apparent at birth, despite the presence of disease on PSG. Second, untreated OSA in children may manifest as failure to thrive instead of obvious airway obstruction (Marcus et al., 1994; Wilson et al., 2000). Third, OSA in combination with known feeding difficulties can further exacerbate growth failure because both OSA and PRS can contribute to feeding difficulty (Shprintzen, 1992). Indeed, a study by Lidsky et al. (2008) found that gastrostomy tube placement for feeding difficulties in PRS was not required in any of the children with isolated PRS who underwent early airway intervention (within the first 3 months of life), whereas 13% of those with no airway intervention or delayed intervention required gastrostomy tube placement. This suggests that early resolution of airway obstruction may ameliorate feeding difficulties in these patients. Fourth, the diagnosis and treatment of OSA is also essential to prevent long-term sequelae such as neurocognitive deficits and cardiovascular disease such as
5 618 Cleft Palate Craniofacial Journal, September 2011, Vol. 48 No. 5 systemic and pulmonary hypertension, right ventricular hypertrophy, and cor pulmonale (Gozal and O Brien, 2004). Limitations of this study include the small sample size and retrospective nature of data collection for the first seven patients. In order to address this, we compared the group of retrospectively collected patients with those who were prospectively collected and found no difference between groups. The mean and individual results for these groups can be seen in Table 1. There may be selection bias in the study population in that the infants with PRS who underwent PSG in the first year of life may differ clinically from those infants with PRS who did not. It is likely that those with snoring and failure to thrive were more prone to be referred for PSG. It is also likely that children without PSG evaluation represent a dichotomous population that includes infants with PRS with mild upper airway obstruction and no noted oxygen desaturation, as well as infants with severe disease who underwent early airway intervention without PSG. CONCLUSION There was a high incidence of OSA in this group, which suggests that OSA may be common in infants with PRS. Results from a cohort of six prospectively collected consecutive patients compared with those from a group of seven nonconsecutively tested patients showed rates of 83% and 86%, respectively, as measured by 16-channel PSG. A majority of these children (6 of 11, or 55%) had severe OSA, with 50% seen in the nonconsecutive group and 60% seen in the consecutive cohort. It is interesting that, whereas snoring is a common indication for the evaluation of sleep disordered breathing, it was an unreliable predictor for the presence of OSA in these children, with 5 of 11 (45%) infants exhibiting no snoring. These findings underscore the importance of polysomnographic screening of infants with PRS for OSA, even in the absence of clinical symptoms of airway obstruction or snoring. In infants with PRS, unrecognized OSA that goes untreated can contribute to feeding difficulties, failure to thrive, and long-term neurologic and cardiovascular sequelae. Future studies should be performed in a prospective fashion to determine the true prevalence of OSA in the PRS infant population and to understand the effects of intervention on upper airway obstruction, feeding difficulty, and growth. In addition, standardized recording of associated symptoms will allow for better determination of which patients are most likely to have OSA. REFERENCES American Academy of Sleep Medicine (AASM). The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. Westchester, IL: AASM; Bravo G, Ysunza A, Arrieta J, Pamplona MC. Videonasopharyngoscopy is useful for identifying children with Pierre Robin sequence and severe obstructive sleep apnea. Int J Pediatr Otorhinolaryngol. 2005;69: Breugem CC, Mink van der Molen AB. What is Pierre Robin sequence? J Plast Reconstr Aesthet Surg. 2009;62: Carroll JL, McColley SA, Marcus CL, Curtis S, Loughlin GM. Inability of clinical history to distinguish primary snoring from obstructive sleep apnea syndrome in children. Chest. 1995;108: Donnelly LF, Strife JL, Myer CM III. Glossoptosis (posterior displacement of the tongue) during sleep: a frequent cause of sleep apnea in pediatric patients referred for dynamic sleep fluoroscopy. AJR Am J Roentgenol. 2000;175: Gilhooly JT, Smith JD, Howell LL, Deschaine BL, Richey SL. Bedside polysomnography as an adjunct in the management of infants with Robin sequence. Plast Reconstr Surg. 1993;92: Gozal D, O Brien LM. Snoring and obstructive sleep apnoea in children: why should we treat? Paediatr Respir Rev. 2004;5(suppl A):S371 S376. Katz ES, D Ambrosio CM. Pathophysiology of pediatric obstructive sleep apnea. Proc Am Thorac Soc. 2008;5: Lidsky ME, Lander TA, Sidman JD. Resolving feeding difficulties with early airway intervention in Pierre Robin sequence. Laryngoscope. 2008;118: Marcus CL, Carroll JL, Koerner CB, Hamer A, Lutz J, Loughlin GM. Determinants of growth in children with the obstructive sleep apnea syndrome. J Pediatr. 1994;125: Meyer AC, Lidsky ME, Sampson DE, Lander TA, Liu M, Sidman JD. Airway interventions in children with Pierre Robin sequence. Otolaryngol Head Neck Surg. 2008;138: Muzumdar H, Arens R. Diagnostic issues in pediatric obstructive sleep apnea. Proc Am Thorac Soc. 2008;5: Robin P. La chute de la base de la langue considérée comme une nouvelle cause de gans la respiration naso-pharyngienne. Bull Acad Natl Med (Paris). 1923;89: Robin P. Glossoptosis due to atresia and hypotrophy of the mandible. Am J Dis Child. 1934;48: Shprintzen RJ. The implications of the diagnosis of Pierre Robin. Cleft Palate Craniofac J. 1992;29: Singer L, Sidotti EJ. Pediatric management of Robin sequence. Cleft Palate Craniofac J. 1992;29: Spicuzza L, Leonardi S, La Rosa M. Pediatric sleep apnea: early onset of the syndrome? Sleep Med Rev. 2009;13: Traeger N, Schultz B, Pollock AN, Mason T, Marcus CL, Arens R. Polysomnographic values in children 2 9 years old: additional data and review of the literature. Pediatr Pulmonol. 2005;40: Wilson AC, Moore DJ, Moore MH, Martin AJ, Staugas RE, Kennedy JD. Late presentation of upper airway obstruction in Pierre Robin sequence. Arch Dis Child. 2000;83:
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