Dysphagia and Nutrition Problems in Infants With Apert Syndrome

Dysphagia and Nutrition Problems in Infants With Apert Syndrome Valerie Pereira, M.Sc., M.R.C.S.L.T., Paul Sacher, R.D., M.B.D.A., Martina Ryan, M.R.C.S.L.T., L.R.C.S.L.T., Richard Hayward, F.R.C.S. Objective: The purpose of this study was to identify and describe the nature of dysphagia and nutrition difficulties in infants with Apert syndrome. Design: The study comprised a review of the medical, nutrition, and feeding records of 13 consecutive infants still feeding by the bottle who had been referred to the Craniofacial Unit and analyses of swallow function from videofluoroscopic swallow investigations. Main Outcome Measures: Outcome measures included qualitative analyses of bottle-feeding and nutritional status and quantitative functional severity ratings of dysphagia based on videofluoroscopic swallow investigations using the O’Neil et al. (1999) Dysphagia Outcome Severity Scale. Results: The main qualitative descriptors of oral feeding in this cohort included uncoordinated suck-swallow-breathe patterns, inability to maintain sucking bursts, and changes in respiratory patterns as the feed progressed. Videofluoroscopic evaluations (N = 7) showed silent laryngeal penetration or aspiration in more than half of the cohort. Failure to thrive was a frequent occurrence seen in seven infants, and 9 of the 10 required dietetic intervention and enteral supplements. (Nutritional records were not located for three infants.) Conclusions: In view of the small sample size and retrospective nature of the study, the results need to be interpreted with caution. However, the study adds to current limited knowledge on feeding and nutrition in Apert syndrome. Further prospective multidisciplinary and objective research is clearly warranted. KEY WORDS:

Apert syndrome, aspiration, bottle-feeding, dysphagia, nutrition, videofluoroscopy swallow

Apert syndrome, or type I acrocephalosyndactyly, is characterized by craniosynostosis (usually acrocephaly or bracycephaly and a high prominent forehead), midface hypoplasia, and symmetrical syndactyly of the hands and/ or the feet (from partial to complete fusions of the digits). Hypoplasia of the midface in this syndrome results in a

short cranial base with a reduction of pharyngeal height (Peterson-Falzone et al., 1981; Kaloust et al., 1997), a narrow nasal cavity, depressed nasal bridge, and a diminished nasopharyngeal space (Cohen and Kreiborg, 1996). In addition, the maxilla is retropositioned and retruded, and there is relative prognathism, resulting in the characteristic Class III malocclusion. Midface hypoplasia in this clinical population also results in irregular positioning of the teeth and dental overcrowding, resulting in the classic anterior open bite and posterior crossbite (Ferraro, 1991; Cohen and Kreiborg, 1996). The hard palate is high, narrow, arched, and short, and the soft palate is long and thick (Peterson-Falzone et al., 1981; Ferraro, 1991). In about 75% of cases, there is a cleft of the soft palate or bifid uvula (Cohen and Kreiborg, 1996). With such an altered oral-facial anatomy, an adverse impact on early feeding in infants with Apert syndrome is to be expected. In addition, abnormalities of the central nervous system including malformations of the corpus callosum and/or limbic structures (Cohen and Kreiborg, 1993b); hindbrain herniation (Gonsalez et al., 1998; Leighton and Lane, 2005); abnormalities with the posterior fossa (Slaney et al., 1996); and cardiovascular, respiratory, and intestinal anomalies (Cohen and MacLean, 2000) have been documented in this syndrome and may contribute to or result in feeding difficulties.

Ms. Pereira is Specialist Speech and Language Therapist in Cleft Lip and Palate/Velopharyngeal Dysfunction, North Thames Regional Cleft Service, London, United Kingdom (previously Specialist Speech and Language Therapist in Craniofacial Conditions/Dysphagia, Craniofacial Unit, Great Ormond Street Hospital for Children NHS Trust, London, United Kingdom). Mr. Sacher is Senior Research Fellow, Institute of Child Health, and Honorary Dietitian, Great Ormond Street Hospital for Children NHS Trust. Ms. Ryan is Specialist Speech and Language Therapist in Dysphagia, Great Ormond Street Hospital for Children NHS Trust, London, United Kingdom. Prof. Hayward is Consultant Pediatric Neurosurgeon, Craniofacial Unit, Great Ormond Street Hospital for Children NHS Trust, London, United Kingdom, and Honorary Senior Lecturer, Institute of Child Health. Parts of this paper were presented at the United Kingdom and Ireland Cleft and Craniofacial Society Conference in Dublin, 2001, and the 4th Asia-Pacific Craniofacial Conference in Tokyo, 2002. Submitted July 2008; Accepted September 2008. Address correspondence to: Valerie Pereira, Specialist Speech and Language Therapist, Speech and Language Therapy Department, Great Ormond Street Hospital for Children NHS Trust, Great Ormond Street, London WC1N 3JH, UK. E-mail [email protected]. DOI: 10.1597/08-010.1 285

286 Cleft Palate–Craniofacial Journal, May 2009, Vol. 46 No. 3

Airway obstruction is a primary functional pathology reported in Apert syndrome. The short cranial base, reduced pharyngeal height, and decreased nasal airway predispose the infant with Apert syndrome to upper airway difficulties (Lauritzen et al., 1986; Perkins et al., 1997; Sculerati et al., 1998; Lo and Chen, 1999). Airway obstruction can include nasopharyngeal obstruction (e.g., choanal stenosis), sleep apnea, and/or respiratory distress syndrome. In addition, some infants with Apert syndrome may have laryngeal anomalies (Cohen et al., 1992). A solid cartilaginous trachea may result in respiratory inefficiency or an inability to clear secretions (Cohen and MacLean, 2000), both of which would have an adverse impact on feeding. Bottle-feeding in Apert Syndrome Bottle-feeding difficulties in infants with midface hypoplasia have been documented in the literature and usually are attributed to airway difficulties (Thompson et al., 1994; Tuchman and Walter, 1994; Posnick, 1996; Brodsky, 1997). Although several studies have shown that nasal breathing in normal infants may not necessarily be obligatory (e.g., Miller et al., 1985; Rodenstein et al., 1985), switching to oral breathing may be done ‘‘at a cost to the infants in terms of efficiency of breathing’’ (Wolf and Glass, 1992, p. 47). When normal nasal breathing is not possible or restricted, as is often the case in Apert syndrome, these infants are thus immediately put at risk for bottle-feeding difficulties (Pereira, 2005). It is well documented in the literature that for safe and successful bottle-feeding to occur, the relationship between the acts of sucking, swallowing, and breathing have to coordinate accurately and effectively with one another. The coordination of pharyngeal and laryngeal musculature with the airway patent for breathing but protected for swallowing also has to be precise (Brodsky, 1997). A difficulty at any stage of this coordination process will have an adverse effect on the other stages of swallowing and puts the infant at risk for laryngeal penetration (‘‘food or liquid penetrating the laryngeal inlet to just above the level of the vocal folds and clearing’’) or aspiration (‘‘food or liquid entering the trachea/airway’’) (Hiorns and Ryan, 2006, p. 918). The possible risks and consequences of aspiration are that the infant’s airway is endangered by the production of mechanical obstruction and bacterial pneumonia, which can result in long-term complications such as recurrent pneumonia and bronchitis (Arvedson and Brodsky, 2002). Bottle-feeding in Apert syndrome is described in the literature as being prolonged with an increase in noisy breathing as the feed progresses, and often, an uncoordinated suck-swallow-breathe pattern is seen (Thompson et al., 1994; Posnick, 1996), resulting in coughing and even choking during feeding (Tuchman and Walter, 1994). Such feeding difficulties may result in inadequate calorie intake and in more severe cases, failure to thrive if not resolved or managed effectively. In a study looking at airway

management in children with midface hypoplasia (including Apert, Pfeiffer, Hallermann-Streiff, Crouzon, and Saethre-Chotzen syndromes and CHARGE association [Perkins et al., 1997]), the authors reported feeding difficulties in about 30% (14 out of 45) of this cohort but provided no details as to the nature of these difficulties. To the authors’ knowledge, there is currently no report of a systematic attempt at identifying and describing the nature of these feeding difficulties or the use of objective methods to assess swallow function in infants with Apert syndrome. Nutrition and Growth in Apert Syndrome The nutritional status of infants with Apert syndrome has not been the subject of detailed study in the literature. It has, however, been noted that infants with syndromic craniosynostosis, including Apert syndrome, may present with nutritional imbalance and failure to thrive if feeding problems are not diagnosed and treated early (Turvey et al., 1996). There is evidence in the literature to show that nutritional impairment in very young infants affects their long-term health, growth, and development (Lucas et al., 2001). With regard to growth, there is currently very little known about general growth in Apert syndrome and longitudinal data are scarce. Cohen and Kreiborg (1993a) showed that mean newborn weight and length of infants with Apert syndrome exceeded the 50th percentile. Cohen and MacLean (2000) found that 16% of their sample (N 5 76) exceeded a birth weight of 4000 g compared with approximately 5% of the general population. This was attributed to megalencephaly, a characteristic of Apert syndrome. Unfortunately, the study only followed growth and did not examine energy expenditure or dietary intake. The two primary aims of the present study were, therefore, as follows: (1) to identify and describe the nature and extent of bottle-feeding and swallow function difficulties in infants with Apert syndrome based on standard feeding parameters evaluated during clinical bedside evaluation and videofluoroscopic swallow investigations; and (2) to identify and describe the nature and extent of nutritional difficulties in infants with Apert syndrome. A secondary aim of the study was to begin to explore possible causes of bottle-feeding and swallow function difficulties in infants with Apert syndrome through qualitative analyses and quantitative severity ratings of dysphagia from videofluoroscopic swallow investigations. MATERIALS AND METHODS A review of medical, nutrition, and feeding records of all new Apert infant referrals (N 5 17) to the Unit over a 3year period was undertaken. The study was registered with Great Ormond Street Hospital NHS Trust/Institute of Child Health, London, as a retrospective chart review at the time of data collation.

Pereira et al., DYSPHAGIA AND NUTRITION PROBLEMS IN APERT SYNDROME 287

TABLE 1

Subject Descriptions at Initial Feeding Assessment Including Information on Cleft and Upper Airway Status

Infants

Gender

Age at Initial Assessment (mo)

1 2 3 4 5 6 7 8 9 10 11 12 13

M F M F M M M F M M M M F

10 14 24 7 2 1 3 7 7 5 6 12 6

Cleft Diagnosis*

cleft of the soft palate (repaired) cleft of the palate cleft of the palate cleft of the palate bifid uvula/posterior cleft none noted notching of the soft palate cleft of the palate cleft of the palate. none cleft of the soft palate none bifid uvula

Upper Airway Status (Due to Choanal Stenosis/Atresia)

yes yes yes yes yes yes yes no yes no no yes no

* More detailed diagnoses of the cleft were not available.

On referral to the Unit, three infants were no longer being fed by the bottle and the fourth was on nil by mouth and received his nutrition via a gastrostomy. All four infants, therefore, were excluded from the final total of 13 consecutive infants, all of whom were still feeding on the bottle at the time of referral to the Unit. Nine were boys and four were girls. The mean age when first seen was 8.4 months (range, 1 to 24 months). Ten infants (77%) had a cleft of the palate. Only one infant (Infant 1) had undergone a cleft palate repair prior to the initial bottlefeeding assessment. Nine infants (69%) were reported to have upper airway obstruction as a result of choanal stenosis or atresia. None of the infants had any active airway intervention on referral to the Unit or on initial clinical bedside evaluation. However, as part of the team management of significant airway difficulties and following initial feeding assessment, four infants went on to have a tracheostomy placed (Infants 3, 6, 7, and 9), and one infant, a nasopharyngeal airway (Infant 5). All five infants were seen consequently for follow-up feeding assessments including videofluoroscopy swallow investigations. Case details including information on cleft and airway status are presented in Table 1. To systematize our observations, a pro forma bottlefeeding assessment was created to collate the relevant data in a coherent manner and to enable us to compare the data across all the infants seen regardless of age when seen (i.e., 1 to 24 months). The pro forma assessment consisted of standard bottle-feeding evaluation parameters as reported in well-known pediatric dysphagia textbooks (e.g., Morris and Klein, 1987; Wolf and Glass, 1992; Arvedson and Brodsky, 2002) and as used by practicing dysphagia therapists in the field. Standard parameters include coordination of sucking, swallowing and breathing, respiratory effort, and swallow function. Operational definitions, adapted from Wolf and Glass (1992) and Arvedson and Brodsky (2002), are provided below.

Coordination of Sucking, Swallowing, and Breathing. The new infant normally has a suck-swallow ratio of 1:1 with a 1- to 2-second pause to breathe. The ratio can change as the feed progresses, and older infants may take

two to three sucks per swallow (Wolf and Glass, 1992). The normal sucking burst ranges from 10 to 30 suck-swallow sequences that decrease nearer the end of a feed (Arvedson and Brodsky, 2002). With a disorganized sequence or uncoordinated suck-swallow-breathe patterns, the clinician may observe variability in the duration of sucking bursts and pauses, or frequent coughing/choking (Wolf and Glass, 1992). Respiratory Effort. Increased respiratory effort or ‘‘work of breathing,’’ is observed through signs such as flaring of the nostrils and chest retraction, as well as premature fatiguing, resulting in the infant falling asleep before the feed is completed (Wolf and Glass, 1992). Increased respiratory effort often compromises the suck-swallowbreathe coordination. Swallow Function. Clinical indicators of swallow dysfunction include coughing/choking during swallowing and noisy breathing. Coughing/choking during a feed may be indicative of possible laryngeal penetration or aspiration and also can signal uncoordinated suck-swallow-breathe patterns (Wolf and Glass, 1992). Noisy breathing relates to the presence of wet- or congested-sounding breathing after a swallow, and if this worsens as the feed progresses and appears to come from the level of the pharynx (as opposed to the nasal cavity/oropharynx), it signals possible pooling or poor/inadequate clearance of the feed (liquid) from the pharynx (Wolf and Glass, 1992). This places the infant immediately at risk of aspiration. These clinical observations would have been made by speech and language therapists specializing either in craniofacial conditions and/or dysphagia and would have been documented in the infants’ medical and/or feeding records. Seven infants (54%) presented with clinical indicators of possible aspiration including overt signs such as coughing or choking during swallowing, laryngeal gurgling, noisy or wet respirations, and/or subtle signs such as recurrent pneumonia chest infections (Wolf and Glass, 1992; American Speech-Language-Hearing Association, 2000; Arvedson and Brodsky, 2002) and therefore were referred on for objective videofluoroscopy swallow investigations.


Videofluoroscopy swallow investigations were undertaken in Radiology by a pediatric radiologist and a speech and language therapist specializing in dysphagia. Videofluoroscopic swallow investigations were analyzed qualitatively according to stages of swallowing (i.e., oral phase, triggering the pharyngeal phase, and the pharyngeal phase), using parameters set out by Arvedson and Lefton-Greif (1998) that provide a comprehensive description of the use of videofluoroscopy swallow investigations within the pediatric population. The functional severity of dysphagia for each infant also was rated using the Dysphagia Outcome and Severity Scale (O’Neil et al., 1999). This particular scale was used because it was developed specifically to rate the functional severity of dysphagia from videofluoroscopic swallow investigations (O’Neil et al., 1999), and to the authors’ knowledge, there are currently no published scales for rating the severity of dysphagia in infants or children. The ratings in this scale are as follows: 1 indicates severe dysphagia; 2 indicates moderately severe dysphagia; 3 indicates moderate dysphagia; 4 indicates mild to moderate dysphagia; 5 indicates mild dysphagia; 6 indicates within functional limits; and 7 indicates normal swallow. Nutritional status was assessed retrospectively by examining dietetic record cards used by dietitians to record nutritional consultations of all the infants. Information collected and recorded included patient demographics, diagnosis, medical history, diet history, weight and percentile, type of formula or feed, method of feeding, and growth status. Nutritional advice given and follow-up data were assessed also. RESULTS From clinical evaluation of bottle-feeding, the most common and frequently reported feeding characteristics were as follows:

N Lack of coordination of the suck-swallow-breathe patN

N

N N

terns. Nasal flaring was evident in at least three infants (25%). Inability to maintain sucking bursts. Frequent pauses were required during feeding, and in at least three infants (25%), the pauses were reported to increase in length toward the end of the bottle-feeding. Changes in breathing patterns as the feed progressed were characterized mainly by noisy breathing or an inconsistent rate of breathing. In two infants (15%), chest retraction was observed and in one infant, head extension. Coughing/choking during feeds was reported in seven infants (54%). Nasopharyngeal reflux was reported in three infants, (23%) and in two of the infants, this was observed to occur only when the infant coughed.

Seven out of the 13 infants (54%) underwent initial videofluoroscopic swallow evaluations due to clinical

FIGURE 1 Functional severity ratings of videofluoroscopy swallow investigations prior to and following active airway intervention (see Table 2 for severity level ratings). *Infant 6 did not tolerate a repeat investigation.

indications of suspected aspiration. Following initial videofluoroscopic swallow investigations, four infants had a tracheostomy placed and one a nasopharyngeal prong to manage their airway difficulties. Because there is evidence to suggest that such active airway intervention (e.g., tracheostomy in situ) can have a negative impact on swallow function (e.g., Abraham and Wolf, 2000; Norman et al., 2007), these five infants (Infants 3, 5, 6, 7, and 9) underwent repeat videofluoroscopy swallow investigations. Qualitative analysis of initial videofluorosopic swallow evaluations (N 5 7) indicated that all seven infants showed poor bolus formation and poor posterior tongue propulsion in the oral phase, delayed swallow onset, pooling in the valleculae and/or pyriform sinus and postswallow residue in the valleculae and/or pyriform sinus in the pharyngeal phase. Aspiration with thin liquids was evident in three infants (Infants 3, 5, and 7) and laryngeal penetration in one infant (Infant 2). Both laryngeal penetration and aspiration in all four infants occurred during the swallow event as opposed to prior to or after the swallow event. None of the infants showed any behavioral response to this laryngeal penetration or aspiration. There was 90% agreement on functional severity ratings of dysphagia for all videofluoroscopy swallow investigations between the two raters. For the initial videofluoroscopy swallow investigations (i.e., where none of the infants had any active airway intervention in situ), all seven infants were rated as having dysphagia, one as moderately severe (level 2), two as moderate (level 3), two as mild to moderate (level 4) and two as mild (level 5). Five infants consequently underwent active airway intervention: four infants had a tracheostomy placed (Infants 3, 6, 7, and 9) and one a nasopharyngeal airway (Infant 5). All five infants were seen for a repeat videofluoroscopy of their swallow function following active airway intervention; however, infant 6 did not cooperate at the repeat swallow investigation (see Fig. 1; Table 2). Infants 7 and 9 showed improvement in swallow function with active airway intervention with a new severity rating of 6 (i.e., functional limits), progressing from previous ratings of 3 (moderate dysphagia) and 5 (mild dysphagia), respectively, prior to active airway intervention. The other two, Infants 3 and 5, showed improvements in their severity ratings; although, both


TABLE 2 Functional Severity Ratings of Videofluoroscopy Swallow Investigations Level

Severity

1 2 3 4 5 6 7

severe dysphagia moderate-severe dysphagia moderate dysphagia mild-moderate dysphagia mild dysphagia within functional limits normal swallow

remained as dysphagic even after active airway intervention. Infant 3 was rated as a 5 (mild dysphagia) and Infant 5 as a 3 (moderate dysphagia). Ten infants were assessed by a pediatric dietitian (no nutrition records were located for three infants). Failure to thrive was seen in seven infants (weight below the 0.4th percentile). Nine infants required dietetic intervention with either concentration of their current infant formula, prescription of a high-nutrient feed, or the addition of an energy supplement to their current milk formula (Table 3). DISCUSSION The aims of this study were to identify and describe the nature and extent of bottle-feeding and swallow function difficulties in infants with Apert syndrome based on standard feeding parameters evaluated during clinical bedside evaluation and videofluoroscopic swallow investigations, as well as to identify and describe the nature and extent of nutritional difficulties in these infants. A secondary aim of the study was to begin to explore possible causes of bottle-feeding and swallow function difficulties in infants with Apert syndrome through qualitative analyses and quantitative severity ratings of dysphagia from videofluoroscopic swallow investigations. We present the clinical findings of 13 infants with Apert syndrome. During bedside clinical evaluation of bottle-feeding, clinical indicators of swallow dysfunction, difficulties with suck-swallow-breathe coordination, and changes in respiratory effort were seen in our cohort of infants with Apert syndrome, similar to what has been reported previously in the literature (e.g., Thompson et al., 1994; Tuchman and TABLE 3

Walter, 1994; Posnick, 1996). These feeding difficulties can be attributed to the infant’s upper airway difficulty. An abnormality with anatomical structures within the nose, nasopharynx, oral cavity, oropharynx, hypopharynx, and/or larynx immediately predisposes the infant to such feeding difficulties and hence, places the infant at risk for laryngeal penetration and/or aspiration of fluid. Oral-facial abnormalities are an inherent part of Apert syndrome, and midfacial hypoplasia in the syndrome results in choanal stenosis and a diminished nasopharyngeal space. In our cohort, nine infants, or almost 70% of the cohort, were noted to have upper airway obstruction as a result of either choanal atresia or stenosis, with five infants requiring active airway management such as a tracheostomy or nasopharyngeal prong. However, one also needs to consider other possible contributing factors including the retruded midface itself, as well as the role of the long, thick soft palate, characteristic in this clinical population. In addition, the infant with Apert syndrome has to contend with a normal-sized tongue within an abnormally small oropharyngeal cavity. During bottle-feeding, the nipple is placed in the infant’s oral cavity, making any accompanying or compensatory mouth breathing difficult or impossible. As the act of breathing becomes problematic for the infant with Apert syndrome, the accurate and effective coordination of the suck-swallow-breathe pattern is affected and consequently, feeding is compromised, resulting in increased risks of aspiration. It is therefore not surprising that with increased respiratory effort or work of breathing during bottle-feeding, failure to thrive and poor weight gain were common in our cohort of infants. This inadequate intake of calories could be associated either with the incompletion of oral feeds due to fatigue or the excessive use of calories during the feed (Wolf and Glass, 1992). As a consequence, 9 of the 10 infants for whom nutritional records were found were reported to have required a highenergy feed, which was individualized and was based on the child’s medical condition and feeding needs. Even the infant who did not present with failure to thrive was given nutritional supplements due to poor weight gain. However, an uncoordinated suck-swallow-breathe sequence also can be a result of a neurological deficit. The

Details of Nutritional Status at Initial Assessment and Consequent Dietetic Intervention of Infants Seen (N = 10)*

Case

Weight (percentile)

Diagnosis of FTT {

Clinical Dietetic Prescription

1 2 3 4 5 6 7 8 9 10

50th ,0.4th ,0.4th ,0.4th 50th 25th %0.4th %0.4th ,0.4th ,0.4th

no yes yes yes no no yes yes yes yes

energy supplement high-nutrient feed plus energy supplement concentrated formula plus energy supplement high-nutrient feed plus energy supplement none high-nutrient feed thickened high-nutrient feed high-nutrient feed and fiber tube feed concentrated formula with added thickener plus energy supplement fortified expressed breast milk, hydrolyzed formula

* Nutritional records were not located for three infants. { FTT indicates failure to thrive (i.e., infant’s weight is below 2nd percentile for weight for age.


limited evidence from videofluoroscopy swallow evaluations in this study provides us with a glimpse of this. Qualitative analyses showed that no attempt to clear the airway was made by any of the three infants who aspirated, indicating ‘‘silent aspiration.’’ None of the three infants made any behavioral response (e.g., coughing), thereby pointing to a possible neurological basis (Arvedson and Lefton-Greif, 1998). Studies have shown the involvement of the brain-stem in the act and coordination of the suckswallow-breathe sequence (e.g., Koizumi et al., 2007). In Apert syndrome, abnormalities with the posterior fossa were found in almost 21% of the subject cohort (Slaney et al., 1996), and hindbrain herniation, which has been documented in Apert syndrome (e.g., Leighton and Lane, 2005), may affect brainstem structures, which can result not only in upper airway obstruction and central sleep apnea but also in feeding and swallowing difficulties (Nickerson, 1992; Gonsalez et al., 1998; Leighton and Lane, 2005). At present, however, the exact nature and relationship between such malformations of the central nervous system and bottle-feeding in Apert syndrome remains relatively illdefined and unexplored (Pereira, 2005). Quantitative analyses of videofluoroscopic swallow evaluations, in the form of severity ratings of dysphagia, provide some evidence (although limited) that even when airway difficulties are managed actively as with a tracheostomy, feeding difficulties may not automatically resolve, suggesting the potential involvement of other factors contributing to feeding difficulties in infants with Apert syndrome. In two of the infants who had a tracheostomy placed, swallow function did not become normalized and both infants remained dysphagic. In conclusion, this small study has enabled us to describe in more detail than previously has been published the nature and extent of bottle-feeding and nutrition difficulties in infants with Apert syndrome. Qualitative and quantitative analyses of videofluoroscopic swallow evaluation have provided us with initial, albeit limited, evidence with which to explore other plausible causes of feeding difficulties in these infants. The numbers in this study are small and the inherent limiting nature of a retrospective type study is acknowledged. The results of this study, therefore, need to be interpreted with caution, and formal conclusions or generalizations cannot be made at this point. The study, however, highlights the need for, and the importance of, a more routine, objective, and systematic method of assessing and managing feeding and nutrition in Apert syndrome. Due to the complex nature of Apert syndrome, a multidisciplinary approach clearly is warranted. Routine investigations including anthropometry, assessments of respiratory and cardiovascular function, and neurological and developmental status are advocated. Prospective and objective research in this area also should consider using standardized feeding scales such as the Neonatal Oral Motor Assessment Scale (Meyer Palmer et al., 1993) and relevant sections of the Schedule of Oral-Motor Assessment

(Reilly, 2000), as well as objective measures including the Great Ormond Street Measurement of Infant Feeding (Masarei et al., 2001, 2007), which allows for the measurement of parameters such as the length of a sucking burst and suck-swallow ratios, and videofluoroscopy swallow evaluations, all obviously subject to ethics approval in the context of a research study. Until then, it is not possible to ascertain the exact causes of feeding and nutritional difficulties in this population and hence to inform regarding the best form of clinical management. Acknowledgments. This study was undertaken while the first author was employed as a Speech and Language Therapist within the Craniofacial Unit. We would like to thank Rebecca Harris, Victoria Thorpe, and Hayley Smithers, specialist speech and language therapists in dysphagia, for their help with the qualitative and quantitative analyses of the videofluoroscopic swallow evaluations in this study.

REFERENCES Abraham SS, Wolf EL. Swallowing physiology of toddlers with long-term tracheostomies: a preliminary study. Dysphagia. 2000;15:206–212. American Speech-Language-Hearing Association. Clinical indicators for instrumental assessment of dysphagia [guidelines]. 2000, Available at: http://www.asha.org/policy. Accessed June 6, 2008. Arvedson J, Brodsky L. Paediatric Swallowing and Feeding: Assessment and Management. Canada: Singular Publishing Group; 2002. Arvedson J, Lefton-Greif M. Paediatric Videofluoroscopic Swallow Studies: A Professional Manual With Caregiver Guidelines. San Antonio, TX: Communication Skill Builders; 1998. Brodsky L. Dysphagia with respiratory/pulmonary presentation: assessment and management. Semin Speech Lang. 1997;18(1):13–22. Cohen MM Jr, Kreiborg S. A clinical study of the craniofacial features in Apert syndrome. Oral Maxillofac Surg. 1996;25:45–53. Cohen MM Jr, Kreiborg S. Growth pattern in the Apert syndrome. Am J Med Genet. 1993a;47:617–623. Cohen MM Jr, Kreiborg S. An updated pediatric perspective on the Apert syndrome. Am J Dis Child. 1993b;147:989–993. Cohen MM Jr, MacLean RE, eds. Craniosynostosis: Diagnosis, Evaluation, and Management. 2nd ed. Oxford: Oxford University Press; 2000. Cohen MM Jr, Russell J, Kreiborg S. Upper and lower airway compromise in the Apert syndrome. Am J Med Genet. 1992;44:90–93. Ferraro NF. Dental, orthodontic, and oral/maxillofacial evaluation and treatment in Apert syndrome. Clin Plast Surg. 1991;18:291–307. Gonsalez SL, Thompson D, Hayward R, Lane R. Breathing patterns in children with craniofacial dysostosis and hindbrain herniation. Eur Respir J. 1998;11:866–872. Hiorns M, Ryan M. Current practice in paediatric videofluoroscopy. Pediatr Radiol. 2006;36:911–919. Kaloust S, Ishii K, Vargervik K. Dental development in Apert syndrome. Cleft Palate Craniofac J. 1997;34:117–121. Koizumi H, Nomura K, Ishihama K, Yamanishi T, Enomoto A, Kogo K. Inhibition of trigeminal respiratory activity by sucking. J Dent Res. 2007;86:1073–1077. Lauritzen DC, Lilja J, Jarlstedt J. Airway obstruction and sleep apnea in children with craniofacial anomalies. Plast Reconstr Surg. 1986;77: 1–5. Leighton S, Lane R. Airway management in syndromic craniosynostosis. In: Hayward R, Jones B, Dunaway D, Evans R, eds. The Clinical Management of Craniosynostosis. London: MacKeith Press; 2005:161– 191. Lo LJ, Chen YR. Airway obstruction in severe syndromic craniosynostosis. Ann Plast Surg. 1999;43:258–264.


Lucas A, Morley R, Isaacs E. Nutrition and mental development. Nutr Rev. 2001;59:S24–S32. Masarei A, Veness J, Sell D, Wade A, Reilly S. Into the mouths of babes. Speech Lang Ther Pract. Winter 2001:11–13. Masarei A, Wade A, Mars M, Sommerlad B, Sell D. A randomized control trial investigating the effect of presurgical orthopedics on feeding in infants with cleft lip and/or palate. Cleft Palate Craniofac J. 2007;44:182–193. Meyer Palmer M, Crawley K, Blanco IA. Neonatal oral-motor assessment scale: a reliability study. J Perinatol. 1993;13:28–35. Miller MJ, Martin RJ, Carlo WA, Fouke JM, Strohl KP, Fanaroff AA. Oral breathing in newborn infants. J Pediatr. 1985;107:465– 469. Morris SE, Klein MD. Pre-Feeding Skills: A Comprehensive Resource for Mealtime Development. Tucson, AZ: Psychological Corporation; 1987. Nickerson B. Control of breathing problems associated with ArnoldChiari malformation. In: Berkerman RC, Brouilette RT, Hunt CE, eds. Respiratory Control Disorders in Infants and Children. Baltimore, MD: Williams & Williams; 1992:271–276. Norman V, Louw B, Kritzinger E. Incidence and description of dysphagia in infants and toddlers with tracheostomies: a retrospective review. Int J Pediatr Otorhinolaryngol. 2007;71:1087–1092. O’Neil MA, Purdy M, Falk J, Gallo L. The Dysphagia Outcome and Severity Scale. Dysphagia. 1999;14:139–145. Pereira V. Feeding in syndromic craniosynostosis. In: Hayward R, Jones B, Dunaway D, Evans R, eds. The Clinical Management of Craniosynostosis. London: MacKeith Press; 2005:311–338.

Perkins JA, Sie KCY, Milczuk H, Richardson MA. Airway management in children with craniofacial anomalies. Cleft Palate Craniofac J. 1997;34:135–140. Peterson-Falzone SJ, Pruzansky S, Parris PJ, Laffer JL. Nasopharyngeal dysmorphology in the syndromes of Apert and Crouzon. Cleft Palate J. 1981;18:237–250. Posnick JC. Craniofacial dysostosis syndromes: a staged reconstructive approach. In: Tuvey TA, Vig KW, Fonseca RJ, eds. Facial Clefts and Craniosynostosis: Principles and Management. London: WB Saunders; 1996. Reilly S. Schedule for Oral Motor Assessment. London: Whurr; 2000. Rodenstein DO, Perlmutter N, Stanescu DC. Infants are not obligatory nasal breathers. Am Rev Respir Dis. 1985;131:465–469. Sculerati N, Gottlieb MD, Zimbler MS, Chibbaro PD, McCarthy JG. Airway management in children with major craniofacial anomalies. Laryngoscope. 1998;108:1806–1812. Slaney SF, Oldridge M, Hurst JA, Morriss-Kay GM, Hall CM, Poole MD, Wilkie AOM. Differential effects of FGFR2 mutations on syndactyly and cleft palate in Apert syndrome. Am J Hum Genet. 1996;58:923–932. Thompson D, Jones B, Hayward R, Harkness W. Assessment and treatment of craniosynostosis. Acta Neurochir (Wien). 1994;120:123–125. Tuchman DN, Walter RS, eds. Disorders of Feeding and Swallowing in Infants and Children. Pathophysiology, Diagnosis, and Treatment. San Diego: Singular Publishing; 1994. Turvey TA, Vig KW, Fonseca RJ, eds. Facial Clefts and Craniosynostosis: Principles and Management. London: WB Saunders; 1996. Wolf LS, Glass RP. Feeding and Swallowing Disorders in Infancy. Assessment and Management. Tucson, AZ: Therapy Skill Builders; 1992.