BACKGROUND AND OBJECTIVE: Neonatal bulbar weakness (BW) has various etiologies and a broad prognostic range. We aimed to report outcomes in a large series of children with neonatal BW and explore the association of orofacial electrodiagnostic data with outcome.
METHODS: We retrospectively reviewed the files of children who presented with facial, lingual, laryngeal, or pharyngeal weakness at birth and who underwent electrodiagnostic studies combining conventional needle electromyography (EMG) of orofacial muscles, blink responses, and EMG during bottle-feeding. Outcome measures included the need for prolonged respiratory assistance and enteral feeding, as well as sensorimotor and cognitive impairments.
RESULTS: Of 175 patients, 73% had developmental disorders, 25% suffered from acquired brain damage, and 2% had no apparent underlying disorders. Motor or mental impairment was observed in 71%; death occurred in 16%. Outcomes were not significantly different when comparing developmental disorders versus acquired brain damage or neurogenic versus normal detection EMG. Abnormal blink responses were associated with higher frequencies of respiratory assistance (P = .03), gastrostomy (P = .025), and death (P = .009); moderate or severe oropharyngeal incoordinations were associated with higher frequencies of respiratory assistance (P = .006), prolonged enteral feeding (P < .0001), and gastrostomy (P = .0002).
CONCLUSIONS: Orofacial electrodiagnostic studies provide supplementary information to help the pediatrician anticipate the management and prognosis of young infants with BW.
- BR —
- blink response
- BW —
- bulbar weakness
- CHARGE —
- coloboma, congenital heart disease, choanal atresia, mental and growth retardation, genital anomalies, and ear malformations and hearing loss
- EMG —
- EMGbf —
- EMG during bottle-feeding
- PRS —
- Pierre Robin sequence
What’s Known on This Subject:
Neonatal bulbar weakness has various etiologies and a broad prognostic range. Outcomes depend on both the severity of orofacial dysfunction and the nature of underlying neuromuscular or central nervous system disorders.
What This Study Adds:
This is the first report of long-term outcomes in a large series of infants with neonatal bulbar weakness, showing a high risk of motor or mental disabilities and death. Orofacial electrodiagnostic studies result in prognostic indicators regardless of underlying disorders.
Newborn infants with bulbar weakness (BW) present with congenital facial, lingual, laryngeal, or pharyngeal dysfunction, alone or in combination, all of which have significant developmental and functional consequences. Individual course may vary from rapid discharge without any sequelae to prolonged dependence on nutritional and respiratory support, disabilities, or death. Various etiologies include neuromuscular disorders involving the motor neuron, neuromuscular transmission, or muscle and cerebral palsies. The evaluation of a child with BW requires that major emphasis be placed on an etiological definition and a reliable prognostic assessment, because outcomes depend on both the severity of orofacial dysfunction and the nature of underlying neuromuscular or central nervous system disorders.1 Although clinical assessments have been developed,2 predicting outcomes remains a challenging task. Available complementary investigations include videofluoroscopy,3 fiber optic endoscopy,4,5 orofacial electrodiagnostic studies, and esophageal manometry.6 By combining conventional detection of orofacial muscles, recording of blink responses (BRs), and functional electromyography (EMG) during bottle-feeding (EMGbf), electrodiagnostic studies have been shown to help diagnose cranial nerve palsies and sucking/swallowing incoordination.7,8 In this work, we report outcomes in a large series of young infants with neonatal BW of diverse causes and explore the association of orofacial electrodiagnostic data with outcome.
For this retrospective study, approval by an institutional ethics committee was waived by our hospital’s review board. We reviewed the database of our pediatric neurophysiology unit over a 15-year period (July 1, 1995, to December 31, 2010). We identified 692 patients who underwent orofacial electrodiagnostic studies before 6 months of age. We excluded 398 patients treated in other hospitals, 22 patients with unilateral facial palsy presumed to be of obstetrical origin, and 14 patients with isolated cleft palate. This left 258 patients with clinical signs of bulbar dysfunction who were treated in our hospital. We excluded 59 patients with strictly isolated Pierre Robin sequence (PRS), and 24 patients were lost to follow-up before 6 months of age. Thus we included 175 patients and collected clinical, radiologic, and genetic data that contributed to their diagnoses. The data were deidentified before analysis. Diagnoses were established after clinical examination by a neonatologist, a maxillofacial surgeon, and a clinical geneticist. Ocular, skeletal, renal, and cardiac malformations were identified by ophthalmologic examination, radiograph, and ultrasound scans. The brain was investigated by ultrasound scan, computed tomography, or MRI. Upper airways were examined using laryngoscopy. A karyotype was obtained for every patient; deletion at 22q11 was tested in 166 patients. Two etiological groups were defined: (1) developmental disorders and (2) acquired brain damage. Group 1 included patients with genetic anomalies, recognizable malformation syndromes,9 inherited metabolic diseases, or birth defects that have not been yet classified as recognizable syndromes. Group 2 included patients with hypoxic ischemic encephalopathy, birth asphyxia, premature birth (<32 weeks), or fetal exposure to toxic agents.
Orofacial Electrodiagnostic Studies
Electrodiagnostic examinations were all performed by 1 author (FR) and were part of every patient’s assessment. In case of premature birth, electrodiagnostic studies were not performed before gestational age 37 weeks. Three methods, elsewhere described in detail, were combined: conventional detection needle EMG,10 BRs,11 and EMGbf.10 In short, conventional detection EMG was used to study face, tongue, and soft palate muscles, at rest and during crying stages. Traces were analyzed manually and classified as normal, neurogenic single or reduced interference pattern, or low amplitude (full interference pattern with maximum amplitude decreased by ≥30%). BRs were recorded in the orbicularis oculi muscle in response to electrical stimulation of the trigeminal supraorbital nerve; the presence of R1 and R2 components and R1 latency were analyzed, considering an asymmetry of ≤3 milliseconds to be normal. EMGbf was used to assess the pattern of suction as well as sucking/swallowing coordination. The technique consists of a 2-channel recording of the genioglossus muscle for the oral phase, as well as the thyrohyoid muscle for the pharyngeal phase, while the infant drinks sugar water from a bottle. A normal pattern features rhythmic spindle-shaped bursts of activity separated by a quiescent period; the 2 muscles alternate regularly. Abnormal patterns define oropharyngeal incoordination as mild, where sucking is present but the alternation between sucking and swallowing is irregular; moderate, where sucking is present but the pharyngeal phase is either synchronous or at random; or severe, where the tongue does not perform rhythmic sucking activity and the pharyngeal phase is either inactive or tonic. Results were classified as: (1) normal oropharyngeal coordination or mild anomalies or (2) moderate or severe oropharyngeal incoordination.
We recorded the need for respiratory assistance (oxygen or noninvasive ventilation for >1 month, tracheostomy) and enteral feeding (tube feeding for >6 months, gastrostomy), motor and sensory disabilities, behavioral disorders, and language and educational skills. Standardized neurodevelopmental evaluation was not possible given the retrospective nature of the study and differences in follow-up periods. Patients were considered disabled when they suffered from cerebral palsy, sensory hearing loss, poor or no language, and inability to follow a scholar course, even in an adapted school. We defined the absence of disability as normal motor development and normal or slightly delayed (≤2 years) school course.
Numeric variables are presented as mean, median, and range; categorical variables are presented as rates. Comparison of 2 independent groups was performed with the Mann–Whitney U test for numeric variables and the Fisher exact test for categorical variables. Comparison PRS of >2 groups was performed with 1-way analysis of variance for numeric variables and χ2 test for categorical variables. All hypotheses were constructed as 2-tailed. A P value <.05 was considered significant.
The series included 175 patients (84 males, 91 females). The most frequent presenting symptoms were the lack of sucking or swallowing and aspiration episodes. BW was frequently associated with facial malformations. On general neurologic examination, main symptoms were hypotonia, lethargy, and limb hypertonia (Table 1). Excluding 8 patients who died before age 6 months, patients were followed up to age 2 years (25/167, 15%), for 2 to 5 years (48/167, 29%), or for >5 years (94/167, 56%). Genealogical data were available for 120 patients, including 18 born to consanguineous parents. A specific diagnosis was established for 134 patients during the first trimester of life (110) or between 3 months and 7 years (24). The remaining patients had unidentified malformation patterns (36) or no apparent underlying disorder (5) (Table 2). Outcomes are shown in Table 1.
Median age at electrodiagnostic examination was 40 days (range 2 to 180, mean 54). Detection EMG distinguished 85 patients without any neurogenic EMG signs and 90 patients with neurogenic EMG signs in muscles innervated by the facial nerve (82), the pharyngeal plexus (56), and the hypoglossal nerve (31). Low-amplitude traces were recorded in soft palate muscles in 36 patients, including 32 with cleft palate. Of 175 patients, BRs were abnormal (45), bilaterally absent (28), or asymmetric (17). EMGbf showed normal coordination or mild abnormalities in 63 of 145 (43%) patients and moderate or severe oropharyngeal incoordination in 82 (57%). Regarding the 30 patients who did not undergo EMGbf, 23 showed clinical conditions precluding all attempts to feed orally, including 8 patients who died.
When comparing etiological subgroups (developmental disorders versus acquired brain damage) outcomes were not significantly different (Table 3). Patients with abnormal BRs showed higher frequencies of respiratory assistance (P = .03), gastrostomy (P = .016), and death (P = .009) than those with normal BRs. Moderate or severe oropharyngeal incoordination on EMGbf was strikingly associated with the need for respiratory assistance (P = .006), prolonged enteral feeding (P < .0001), and gastrostomy (P = .0004) (Table 4).
By assessing bulbar pathways and oropharyngeal coordination, orofacial electrodiagnostic studies give relevant indicators for the management and prognostic evaluation of young infants with BW. Of 175 infants, their underlying disorders notwithstanding, BW frequently had poor outcome, since 16% of the patients died and more than two-thirds suffered from motor or mental disabilities. Comparing patients with developmental disorders and those with acquired brain damage, the absence of statistically significant differences in outcomes suggests that BW by itself underlies long-term functional and developmental consequences. The small number of patients without apparent underlying disorders did not enable statistical comparisons; of the 5, only 1 required prolonged enteral feeding and none suffered from disability, as usually observed.12 We acknowledge that our series did not include any case of hereditary motor neuropathy, congenital myopathy, or congenital myasthenia syndrome. In patients with cleft palate, low-amplitude myopathic EMG signs detected in soft palate muscles did not reveal myopathic disease but indicated localized developmental muscular hypoplasia. When studying patients with specific diagnoses recognizable at birth, such as coloboma, congenital heart disease, choanal atresia, mental and growth retardation, genital anomalies, and ear malformations and hearing loss (CHARGE syndrome); Moebius syndrome; first arch syndromes; or congenital myasthenic syndromes, different authors found widely varying or facial dysfunctions and outcomes.13–17 For patients with acquired brain damage, a possible association between early sucking and swallowing abilities and neurodevelopment outcome is still open to debate.18 In a recent series of preterm infants, abnormal sucking behavior at 46 weeks of postmenstrual age was associated with neurodevelopment delay.2 Thus, a prognostic evaluation of neonatal BW remains a challenge for the pediatrician.
Video fluoroscopy and fiber optic endoscopy are commonly used to evaluate oropharyngeal dysfunction, but to our knowledge, the association of their results with long-term outcomes has not yet been established. In our practice, in the last 20 years, the use of videofluoroscopy before age 6 months has progressively declined owing to the risk of aspiration and radiation exposure. Meanwhile, electrodiagnostic studies of bulbar muscles and cranial nerves have become a routine diagnostic tool to look for bulbar involvement and investigate the mechanism and severity of dysphagia. These bulbar electrodiagnostic studies investigate paired cranial nerves VII, IX to X, and XII; the V to VII internuclear pathways; and the central pattern generator for swallowing involving the nucleus of the tractus solitarius and adjacent ventromedian reticular formation.19 To that end, orofacial electrodiagnostic studies explore small-sized brainstem structures and cranial nerves that are not routinely studied by using MRI.20,21 Among patients suffering from congenital facial malformations, electrodiagnostic studies have revealed the neurologic origin of dysphagia, even in the absence of neurologic signs or abnormalities in brain images.7 EMG of the genioglossus muscle has detected associated hypoglossal nerve involvement in children with periventricular leukomalacia or hemorrhagic infarction.22 In patients with PRS, the absence of neurogenic EMG signs in orofacial muscles characterized isolated PRS, and EMGbf has contributed to assessing the severity and potential duration of dysphagia.8 Among patients with congenital multiple cranial neuropathy, detection EMG could identify bulbar involvement in patients with orofacial dysfunctions attributed to a suprabulbar vascular insult at preterm or term birth.23
In the present series, neurogenic EMG signs were detected in half of the patients. Curiously, frequencies and durations of respiratory assistance and enteral feeding were not statistically different in patients with or without cranial nerve involvement. These results could be explained by the predominant involvement of cranial nerve VII, whereas airway obstruction and aspiration result from disorders of nerves IX to X and XII. Interestingly, BR abnormalities were significantly associated with high frequencies of respiratory assistance, gastrostomy, and death. BRs explore pathways in close proximity to the respiratory and swallowing centers and running through the reticular formation. The R1 component of BRs corresponds to an oligosynaptic reflex arc involving 2 or 3 synapses in the pons between the main sensory nucleus of cranial nerve V and the motor nucleus of the ipsilateral cranial nerve VII. The R2 component follows polysynaptic medullary pathways, which are more caudal and closer to the bulbar formations. Moreover, EMGbf identified patients with moderate or severe oropharyngeal incoordination, who showed more need for respiratory assistance, long-lasting enteral feeding, and gastrostomy than patients with normal coordination or mild abnormalities. Finally, orofacial electrodiagnostic studies resulted in prognostic indicators of neonatal BW, regardless of the underlying neuromuscular or suprabulbar disorders.
This study has a limitation. Despite the large number of patients we investigated, one can appreciate that 15 years is a long spell of time, and that diagnostic abilities and management have improved. In fact, however, our investigating protocol remained the same during that period, and all patients were able to benefit from recent diagnostic genetic tools.
Early orofacial electrodiagnostic studies do provide the pediatrician with supplementary information, helping anticipate the outcome of BW, given that even if identified at birth, etiology is not the only prognostic indicator.
- Accepted September 30, 2015.
- Address correspondence to Francis Renault, MD, Unité de Neurophysiologie clinique de l’enfant, Hôpital Armand-Trousseau, 28 avenue Arnold-Netter, 75571 Paris 12, France. E-mail:
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: No external funding.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
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- Copyright © 2016 by the American Academy of Pediatrics