Tongue Dysmorphology in Craniofacial Microsomia

PEDIATRIC/CRANIOFACIAL Tongue Dysmorphology in Craniofacial Microsomia Elliott H. Chen, M.D. Russell R. Reid, M.D., Ph.D. Chuma Chike-Obi, M.D. Nancy Minugh-Purvis, Ph.D. Linton A. Whitaker, M.D. Jacek Puchala, M.D. Scott P. Bartlett, M.D. Philadelphia, Pa.; Chicago, Ill., and Krakow, Poland

Background: Craniofacial microsomia is one of the most common and wellcharacterized craniofacial anomalies. Tongue dysmorphism, however, has been neither thoroughly investigated nor reported in the context of this disease. This review focuses on the true prevalence of tongue dysmorphology in craniofacial microsomia and its relation to the deformities seen in this condition. Methods: A 20-year retrospective study was performed to determine the number of patients who had a documented tongue anomaly and any relation to the development of abnormal speech. In recognition of the limitations of this approach, a 1-year prospective study was also performed to see the true prevalence of tongue dysmorphology in these patients. Results: Eight of 167 patients (4.8 percent) in the retrospective study were found to have tongue dysmorphologies, as opposed to 24 of 55 (43.6 percent) in the prospective study. The majority of tongue anomalies were mild. Of the eight retrospective patients, seven currently have intelligible speech with a combination of intensive speech therapy and/or surgical correction. The eighth patient is without intelligible speech. Tongue dysmorphology was positively correlated with the degree of hard- and soft-tissue deformity. Conclusions: Tongue dysmorphologies in craniofacial microsomia, although usually mild, are frequently overlooked. The correlation of the tongue, soft tissue, and mandible anomalies may point to a common error early in gestation or an interdependence of adjacent growth centers. (Plast. Reconstr. Surg. 124: 583, 2009.)

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raniofacial microsomia is one of the most common congenital craniofacial malformations, second only to cleft lip and palate in frequency. Affecting the bony skeleton and soft tissues, its manifestations can vary from mild to severe. Such variable findings have necessitated a host of classification schemes,1–5 multidisciplinary care, and a variation in treatment protocols.6 –10 Although the external features and manifestations of craniofacial microsomia have received detailed attention, there has been less emphasis on the intraoral findings in these patients. Interestingly, to the best of our knowledge, tongue From the Division of Plastic Surgery, The Children’s Hospital of Philadelphia, University of Pennsylvania; the Section of Plastic and Reconstructive Surgery, Comer Children’s Hospital at the University of Chicago Medical Center; and the University Children’s Hospital of the Jagiellonian University. Received for publication August 14, 2008; accepted January 12, 2009. Presented at the International Society of Craniofacial Surgery meeting, in Salvador, Brazil, August of 2007. Copyright ©2009 by the American Society of Plastic Surgeons DOI: 10.1097/PRS.0b013e3181addba9

dysmorphism has not been associated with or described in the spectrum of the deformity. Over the years, a number of patients with craniofacial microsomia have been noted to have anomalies of the tongue. These were observed either during clinical examination in infancy or by referring speech pathologists. This prompted us to perform a retrospective review of our records and a prospective study of patients seen over a 12-month period. Our goal was to determine the true prevalence of tongue dysmorphism and its contribution to speech deformity in our population. Furthermore, we evaluated which features of craniofacial microsomia most correlated with the severity of tongue dysmorphology observed. Finally, we have proposed a classification system for tongue anomalies based on their severity.

Disclosure: None of the authors has any commercial or financial associations that might pose or create a conflict of interest.

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Plastic and Reconstructive Surgery • August 2009 PATIENTS AND METHODS The study, approved by The Children’s Hospital of Philadelphia Institutional Review Board, was divided into two parts: a retrospective chart review and a prospective examination of all clinic patients within a 12-month period. For the first portion of the study, patients with a diagnosis of craniofacial microsomia from 1986 to 2006 were identified through our database. Clinic notes were reviewed carefully for any mention of tongue dysmorphology. Age, gender, diagnosis, speech pathology and therapy findings, surgical interventions, and the most current speech outcomes were noted. Orbit, mandible, eye, facial nerve, and soft tissue (OMENS)3 data were not collected because of the variability in documentation over the 20year time period. No correlation analysis was performed on the retrospective data because of this variability in OMENS and tongue data collection. For the prospective phase of our study, all patients who arrived in the clinic during a con-

secutive 12-month span (July of 2006 to June of 2007) with craniofacial microsomia were examined meticulously for tongue anomalies. Each identified patient was categorized using the OMENS classification system.3 Tongues were classified using the following method: Tng0, normal tongue; Tng1, mild dysmorphisms (such as midline ankyloglossia or unilateral hypoplasia); Tng2, severe dysmorphisms (such as lateral ankyloglossia with fusion to the mandible or severely bifid tongues); and Tng3, total absence of the tongue (aglossia) (Fig. 1). In the cases with bilateral involvement, only the more affected side was counted. If available, speech therapy notes were reviewed. Any patient unable to comply with the examination, with incomplete OMENS scores, or with unknown prior tongue procedures was excluded from the study. All patients and their parents gave verbal consent according to the institutional review board protocol. Patients who were examined

Fig. 1. Photographs of tongue dysmorphology and tongue classifications. Note the relative immobility of the tongues designated Tng 2 (severe dysmorphisms). (Above, left) Tng 1 (mild dysmorphisms): unilateral hypoplasia on the right. (Above, right) Tng 1 (mild dysmorphisms): ankyloglossia and unilateral hypoplasia on the left. (Below, left) Tng 2 (severe dysmorphisms): lateral ankyloglossia with fusion to the mandible on the right. (Below, left) Tng 2 (severe dysmorphisms): bifid tongue.

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Volume 124, Number 2 • Tongue Dysmorphism in the clinic multiple times during the accruement period only had their initial visit counted. If corrective procedures had already been performed for the patient’s craniofacial microsomia, the OMENS classification was established by documentation, radiographs, and photographs from their initial visit. If a full set of OMENS data could not be obtained using these methods, the patient was excluded from the study. Significant positive or negative correlation between the OMENS and tongue score was identified using the Spearman rank order test.11

RESULTS In the retrospective portion of the study, a total of 167 patients were identified with craniofacial microsomia over the 20-year period. A meticulous review of their charts revealed that only eight of these 167 patients (4.8 percent) had any documented tongue dysmorphology (Table 1). Three of the patients were described as having mild dysmorphisms (two with ankyloglossia and one with unilateral hypoplasia), and five of the patients were described as having a severe dysmorphism anomaly (three with lateral ankyloglossia with fusion to the mandible and two with severely bifid tongues) (Table 2). There were no patients with total absence of the tongue identified. Three of the severe dysmorphism patients and one mild dysmorphism patient underwent surgical correction of their tongue anomalies (Table 3.) Seven of eight of these patients had a diagnosis of either bilateral facial microsomia or Goldenhar syndrome. Mandibles in seven patients were Pruzansky grade II or III. No attempt was made to correlate the degree of mandible anomalies with the severity of tongue deformities, as the Pruzansky classifications in the total population of 167 patients were recorded inconsistently and incompletely. Table 1. Retrospective and Prospective Data of Patients with Craniofacial Microsomia Seen at The Children’s Hospital of Philadelphia

No. of patients No. of tongue dysmorphologies Diagnoses Unilateral CFM Bilateral or Goldenhar syndrome CFM, craniofacial macrosomia.

Retrospective Study (1986 –2006)

Prospective Study (2006 –2007)

167

55

8 (4.8%)

24 (43.6%)

Speech evaluation in these patients revealed that seven of eight children (87.5 percent) had speech delays or deficits; in one of these patients, no intelligible speech was present. Five patients underwent speech therapy. Except for the child without speech, all eight patients had resolution of their speech problems; in the most recent evaluation for the seven vocal patients, all were noted to have intelligible speech, with one being hypernasal. In the prospective arm of this study, 65 patients, ranging in from 3 months to 17 years, were identified over the 12-month period. Ten of these patients were excluded because of incomplete OMENS classifications or inability to comply with the intraoral examination. Of the remaining 55, 24 (43.6 percent) were found to have tongue dysmorphisms (Table 1). Nineteen of these were designated to be mild dysmorphism anomalies (13 with unilateral hypoplasia, five with ankyloglossia, and one with a slightly bifid tongue), and the other five were designated severe dysmorphisms (three with lateral ankyloglossia with fusion to the mandible and two with severely bifid tongues) (Table 2). There were no total absence of the tongue anomalies identified. Twenty-nine patients were diagnosed with unilateral craniofacial microsomia, and the remaining 26 were diagnosed with either bilateral craniofacial microsomia or Goldenhar variant. Twenty-one of 55 patients (38.2 percent) were identified as having speech deficits (Table 4). However, only the older patients truly received adequate evaluation. Nineteen were too young to be evaluated. Four were deaf or had no observable speech. Each OMENS category was evaluated individually for correlation to the severity of tongue deformity using the Spearman rank order test. For a 55– data point set, a value greater than 0.266 is equivalent to a value of p ⬍ 0.05; a positive value shows a direct correlation; a negative value, an inverse correlation. A significant direct correlation was found between the severity of lingual deformity and that of the mandible and soft tissue (Table 5). No correlation existed between the severity of lingual deformity and that of the ear or facial nerve. Orbital deformities showed a strong trend toward correlation with tongue dysmorphology but were not statistically significant (p ⫽ 0.060).

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DISCUSSION

7

26

The tongue, in keeping with the rest of the craniofacial skeleton, begins its development early

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Plastic and Reconstructive Surgery • August 2009 Table 2. Classification of Tongue Findings and Distribution within the Craniofacial Microsomia Population Tongue Classification

Retrospective Study (1986 –2006)

Prospective Study (2006 –2007)

3 1 2 0

19 13 5 1 (mild bifidity)

5 3 2

5 3 2

0 0

0 0

Tng 1 Total no. Unilateral hypoplasia Ankyloglossia Other Tng 2 Total no. Lateral ankyloglossia with mandibular fusion Severe bifidity Tng 3 Total no. Congenital absence

Tng1, mild dysmorphisms (such as midline ankyloglossia or unilateral hypoplasia); Tng2, severe dysmorphisms (such as lateral ankyloglossia with fusion to the mandible or severely bifid tongues); Tng3, total absence of the tongue (aglossia).

in the gestational process. At week 4, the tongue starts as two lateral swellings and a single median swelling at the ventral portion of the first pharyngeal arch. Caudal to the median swelling, the tuberculum impar, lays the copula, a medial ventral structure derived from the second, third, and fourth pharyngeal arches. The foramen cecum marks the location between the tuberculum impar and the copula. The lateral lingual swellings grow and overtake the tuberculum impar, forming the mobile anterior two-thirds of the tongue. The copula forms the posterior third, or root, of the tongue. The tongue musculature, with the exception of the palatoglossus, is derived from occipital somites. These somites, which also contribute to the third and fourth arches, migrate into the developing tongue, bringing along their innervation from the hypoglossal nerve.12,13 Congenital tongue anomalies are said to occur as isolated events or as part of a clinical syndrome. Both nonsyndromic and syndromic tongue deformities take the form of aglossia, microglossia, macroglossia, ankyloglossia, clefting, bifidity, or duplications.14 –16 Poor mobility of the tongue, which is inherent in clefting and fusion-type disorders, may impair vital functions of this intraoral appendage, such as mastication, deglutition, and speech. Tongue deformities have been reported to account for misarticulation, double articulation, and overall compromise in speech intelligibility.17,18 The diverse embryologic origins of the tongue, from somites to pharyngeal arches, suggest an equally diverse correlation with other congenital anomalies that develop from the same structures or at the same time during gestation. Tongue anomalies have been associated with limb defects, situs inversus, and asplenia.19 –22 As ex-

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pected, there are case reports of tongue dysmorphology in conjunction with mandibular anomalies, one reported as early as 1845.23–25 Our study confirms this correlation. There was a definite positive relationship between the severity of the mandibular deformity and of the tongue anomalies in the prospective arm of our study. This corroborates with the original OMENS classification study that found a tendency of the most severely affected mandibles to have deficits in all other anatomical areas.3 That study also found that severe soft-tissue anomalies similarly correlated with the severity of the deformities in all anatomical areas except for the ear. Soft-tissue anomalies (exclusive of the ear) were also positively correlated with tongue deformities in our study. The cause of these tongue deformities in craniofacial microsomia is speculative. As the tongue musculature and face have separate embryologic origins (occipital somites and pharyngeal arches, respectively), an association between deformities could signify a common neural crest cell anomaly even before their segmental emigration. Alternatively, given the fact that both the mandible and the anterior tongue (excluding the tongue musculature) originate from the first pharyngeal arch, the coassociation of tongue anomalies and mandibular hypoplasia could be explained as a malformation event. Moreover, the Moss “functional matrix” theory can be applied to the interdependence of bony and lingual soft tissue for normal growth: without a normal tongue, the mandible fails to develop in a normal fashion and vice versa. Stated differently, if the mandible is severely hypoplastic or completely absent, such as in a Pruzansky grade IIb or III mandible, the tongue will fail to receive the normal developmental signals. Conversely, failure in tongue mucosal

Goldenhar syndrome

Goldenhar syndrome Bilateral facial microsomia

Goldenhar syndrome

Hemifacial microsomia

Male

Female

Female

Male

I

III bilaterally

III bilaterally

II bilaterally

III on right, II on left

Tongue ankyloglossia to right mandible; redundant mucosal tissue in floor of mouth Asymmetric frenulum; palatal dysmotility

Bifid tongue, severe ankyloglossia at lingual frenulum

Alveolar cleft; midline bifid maxillary frenulum with tethering and a midline diastasis; tongue ankyloglossia Submucous cleft and tethering of the left hemipalate; fusion of tongue to left hemimandible Hypoplastic tongue with ankyloglossia; paramedian incomplete cleft of tongue Severe ankyloglossia

Tng1

Tng2

Tng2

Tng2

Tng2

Tng2

Tng1

Tng1

Tongue Class

No phonation problems Mild deficits but within normal limits

Mild deficits in speech; developmental articulation errors

Progressive speech delay and velopharyngeal insufficiency

Delayed articulation; developmental speech sound errors Mild delays in expressive language acquisition at 18 mo

Speech Evaluation

None

Developed mild hypernasality and articulation errors after 4 yr 3 mo

Repair of cleft tongue with Zplasty; release of ankyloglossia at 4 yr 10 mo Redundant oral Patient without tissue excised at intelligible speech 2 yr

None

None

Release of the tongue base contracture at 2.5 yr

Release of bifid maxillary frenulum with Z-plasty; lingual frenulum release at 9 mo

None

Surgery for Tongue Abnormality

Yes

N/A

Yes

N/A

Yes

Yes

No

Yes

Speech Therapy

Mild hypernasality, VPI, lisp

N/A

N/A

N/A

Intelligible with occasional w/r substitutions; sibilant distortion from retainer Some s/sh substitutions; d/j substitutions; normal at 6 yr

Normal at 30 mo

Normal at 8 yr

Resolution of Speech Problems

Tng1, mild dysmorphisms (such as midline ankyloglossia or unilateral hypoplasia); Tng2, severe dysmorphisms (such as lateral ankyloglossia with fusion to the mandible or severely bifid tongues); Tng3, total absence of the tongue (aglossia); VPI, velopharyngeal insufficiency.

Male

Bilateral facial microsomia

Male

II bilaterally

Bilateral facial IIA on left, I on microsomia; right bilateral Tessier no. 7 clefts; Tessier no. 0 cleft

Female

IIA on right only Unilateral hypoplasia and palatal dysmotility

Pruzansky Grade

Goldenhar syndrome

Diagnoses

Female

Gender

Oral/Intraoral Finding

Table 3. Longitudinal Data Collected on the Speech Outcomes of the Eight Patients Identified in the Retrospective Arm of the Study

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Plastic and Reconstructive Surgery • August 2009 Table 4. Speech Therapy Evaluations of the 55 Patients Seen in the 1-Year Prospective Arm of the Study No. (%) Normal speech Articulation errors/hypernasality/hyponasality Deaf/no intelligible speech Too young to evaluate Total

11 (20.0) 21 (38.2) 4 (7.27) 19 (34.5) 55

Table 5. Spearman Rank Order Correlation Test Comparing OMENS Classification with Tongue Anomalies Orbit Mandible Ear Facial nerve Soft tissue

Correlation Coefficient

p Value

0.212 0.527 –0.157 –0.071 0.464

0.060 ⬍0.001 0.125 0.303 ⬍0.001

or musculature development may have a downstream adverse effect on mandible growth. The actual prevalence of tongue dysmorphology with craniofacial microsomia is probably underestimated. In our retrospective review, only 4.8 percent of the patients were noted to have anomalies. In our prospective study in which careful scrutiny of the tongue was performed, 43.6 percent of the patients were found to have some type of dysmorphology, with the most common being unilateral hypoplasia of the tongue. Although we observed no cases of aglossia in this series, we have included a class for total absence of the tongue, realizing that deformities of this severity may occur in craniofacial microsomia, but as of yet we have not observed any. It is important to note, however, that other case reports have documented aglossia in the setting of mandibular anomalies.24 In summary, the profound majority of these cases were mild (Table 2) and are typically overlooked on gross examination. This fact is captured by the difference between retrospective and prospective arms of this current study. Thus, regular intraoral examination is a mandate in patients who carry a diagnosis of craniofacial microsomia. We found a significant number of patients with speech difficulties; 87.5 percent of patients in the retrospective arm and 38.2 of percent in the prospective arm were found to have speech deficits. However, use of the Spearman rank order test to determine correlation was impossible because of the high number of patients who were too young to be properly evaluated in the 12-month period of the prospective study. It is difficult to

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draw any type of causality between tongue dysmorphology and speech deficits. The craniofacial microsomia population is known to have an approximate 33 percent incidence of velopharyngeal insufficiency26,27 and a 50 percent incidence of a unilateral hypodynamic palate.28 –30 In our retrospective study, four of eight patients (50 percent) underwent tongue release. Because the majority of these patients also underwent extensive speech therapy, it is difficult to determine what effect this surgical release had on the speech deficits. Clearly, tongue anomalies in the context of an abnormal mandible, lateral facial clefts, palatal clefts, and the like, which is frequently seen in craniofacial microsomia, must be considered additive to the entire speech deficit.

CONCLUSIONS To the best of our knowledge, this is the first study proving a correlation between craniofacial microsomia and tongue dysmorphology. Given the mild nature of the majority of these cases, tongue anomalies are probably often overlooked in the affected infant. The high prevalence (43.6 percent in our prospective study) mandates careful intraoral examination in all patients with craniofacial microsomia. In addition, perhaps the time has come to consider expanding the OMENS classification. OMENTS, TOMENS, and even MENTOS come to mind—the reader can make his or her own choice. Scott P. Bartlett, M.D. The Children’s Hospital of Philadelphia University of Pennsylvania 34th Street and Civic Center Boulevard Philadelphia, Pa. 19104 [email protected]

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