Dysphagia associated with presumed pharyngeal dysfunction in 16 neonatal foals
Reasons for performing study: Dysphagia due to pharyngeal dysfunction occurs in human neonates and is associated with prematurity and hypoxic episodes. This syndrome probably occurs in neonatal foals but has not been reported.
Objectives: The objectives of this study were to describe 1) a series of neonatal foals with dysphagia due to pharyngeal dysfunction; 2) the progression, treatment and resolution of the dysphagia; 3) the comorbidities; and 4) the prognosis for life and athleticism for affected foals.
Methods: Records from 3 referral equine hospitals were reviewed from neonatal foals with dysphagia of pharyngeal origin. Inclusion criteria were a normal to strong suckle, dysphagia evidenced by milk at the nostrils after nursing the dam, and endoscopic examination of the airway. Foals with mechanical reasons for dysphagia, botulism or hyperkalaemic periodic paralysis were not included.
Results: Sixteen neonatal foals qualified for the study. Eight (50%) were premature and/or diagnosed with hypoxic ischaemic encephalopathy. Twelve (75%) had aspiration pneumonia. Fifteen foals were discharged alive from the hospital, nursing the mare with no evidence of dysphagia (n = 14), or mild dysphagia (n = 1), a mean ± s.d. of 7 ± 6 days (median = 6.3 days, range 0–22 days) after hospital admission. One foal was subjected to euthanasia in hospital. Follow-up information was available for 14 animals. Thirteen of 16 (81%) were alive and included one yearling and 12 horses >2 years old. Seven of the 14 (50%) were racing, training or in work, and 6 horses were pets, breeding animals or had unknown athletic status. Two had laryngeal deficits. One foal was subjected to euthanasia within weeks of discharge from the hospital due to aspiration pneumonia.
Conclusion: Dysphagia related to pharyngeal dysfunction occurs in equine neonates and can resolve, but may require days to weeks of supportive care. Prognosis for life is favourable and for athleticism fair.
Swallowing is a complex action involving 26 muscles and 5 cranial nerves (Derkay and Schechter 1998). Dysphagia, or difficulty swallowing, is defined as any defect in the ingestion or transport of endogenous secretions, food or water from the oral cavity to the distal oesophagus (Gryboski 1965). Deficiencies in the oral, pharyngeal or oesophageal phases of mastication or swallowing can cause dysphagia. Because breathing and swallowing share common pathways, aspiration of liquid or solid material may occur with dysphagia. During swallowing and breathing, an ultimate crossing of inspiration and food/liquid pathways occurs in the pharynx, as the bolus moves caudally and dorsally into the oesophagus past the larynx. Muscle actions and coordination are most complex during the pharyngeal phase of the swallow (Derkay and Schechter 1998).
Three important, well-coordinated events occur during swallowing: 1) glottis closure; 2) opening of the cranial oesophageal sphincter by relaxation of the cricopharyngeus muscle; and 3) reflex inhibition of breathing (Gryboski 1965; Derkay and Schechter 1998). Pharyngeal dysphagia occurs when a portion of the effective transport or airway protection is compromised (Logan and Bosma 1967). When the pharyngeal phase of the swallow is incompetent, material may appear in the nares and/or contaminate the lower airway (Bellmaine et al. 1972). Nasal regurgitation is especially prevalent in dysphagic horses because of the position of the soft palate relative to the larynx and the minimal and dynamic nature of the hypopharynx or communication between the oro- and the nasopharynx. Laryngeal contamination generally stimulates coughing in adults, protecting the lower airway (Praud and Reix 2005; Thatch 2007). However, airway protection in neonates may not include cough and may not be stimulated by milk within the larynx (Praud and Reix 2005; Thatch 2007). Cough is produced by chemical or mechanical stimulation of the laryngeal mucosa, initiating the laryngeal chemoreflexes via afferent branches of the superior laryngeal nerve. In neonates (humans, dogs, cats, monkeys and sheep), these reflexes cause mostly swallowing, some apnoea and glottis closure (Praud and Reix 2005; Thatch 2007). Cough is uncommon and may not develop for weeks to months, although a gag response may be present (Praud and Reix 2005; Thatch 2007). The time required for development of the cough reflex in the foal is unknown. The absence or limited nature of the cough as part of the chemoreflexes stimulated by laryngeal contamination places dysphagic neonates at increased risk of pulmonary contamination and aspiration pneumonia (Bellmaine et al. 1972).
As in human neonates, dysphagia probably occurs in neonatal foals due to pharyngeal muscle dysfunction. Transient pharyngeal weakness reportedly arises in some human infants because of inadequate maturation (Gryboski 1965). These infants generally improve with time and their swallowing becomes normal 2–3 weeks after birth (Gryboski 1965; Kilman and Goyal 1976). Interestingly, this dysfunction may be weakness, incoordination or a combination of motor and sensory underdevelopment that may be central and/or peripheral in origin (Gryboski 1965; Kilman and Goyal 1976; Gewolb and Vice 2006). Risk factors for dysphagia due to pharyngeal dysfunction in human infants include prematurity, low birth weight and hypoxic episodes (Gewolb et al. 2001; Gewolb and Vice 2006). Neonatal dysphagia in foals results from cleft palate or soft palate masses, oesophageal disease including megaoesophagus or oesophageal stricture, or primary muscle or central neurological disease, including hyperkalaemic periodic paralysis (HYPP) (Traub-Dargatz et al. 1992). Dysphagia primarily due to pharyngeal dysfunction probably occurs in foals. Providing horse owners with information regarding prognosis for life and athleticism, as well as time in hospital, is critical. Therefore, the purpose of this study was to describe a series of neonatal foals with dysphagia due to pharyngeal dysfunction; the treatment, progression and resolution of the dysphagia; the comorbidities; and the prognosis for life and athleticism.
Materials and methods
Medical records from 3 referral hospitals for neonatal foals admitted with a complaint of dysphagia from 2000 to 2010 were reviewed. Inclusion criteria were dysphagia of pharyngeal origin evidenced by milk at the nostrils and/or within the trachea after nursing the dam with a normal to strong suckle. Foals with cleft palates, soft palate cysts or masses, oesophageal strictures, cysts or megaoesophagus, other congenital anomalies or guttural pouch diseases were excluded. Foals diagnosed with botulism or homozygous (H/H) for HYPP were excluded. Data abstracted from the medical record included case details, age at the time of hospital admission, gestational age (premature <320 days, term = 320–350 days, post term >350 days), clinical evidence of prematurity or dysmaturity, including low birthweight, silky hair coat, domed forehead and/or tendon laxity or clinical evidence of hypoxic ischaemic encephalopathy (HIE) (Rossdale and Short 1967; Hintz et al. 1979; Rossdale 1993; Lester 2005; MacKay 2005). Physical examination data at the time of hospital admission that were evaluated included rectal temperature, respiratory rate, heart rate and presence of a normal or strong suckle. Clinicopathological data obtained at hospital admission were packed cell volume (PCV), total solids (TS), plasma glucose and IgG concentration. Immunoglobulin was determined by quantitative turbidoimmunometric assay on an automated analyser (Hitachi 911 systema; Olympus AU 640-Eb; Roche Cobas Myra PLUSc). Information concerning diagnostic imaging of the airways was reviewed and included airway endoscopy (nasal passages, nasopharynx, larynx and trachea, but not routinely guttural pouches or oesophagus), thoracic and laryngeal/pharyngeal radiography, and thoracic ultrasonography. Data collected regarding patient management included parenteral antimicrobial agents and anti-inflammatory medications administered, and parenteral and/or enteral nutrition. Time to nurse without evidence of aspiration established based on tracheal noise while swallowing or milk at the nares was assessed by the attending clinician. Surgical intervention including laryngotomy or tracheotomy was documented. Number of days in hospital and survival to hospital discharge were recorded. Follow-up information was obtained by accessing Jockey Club (http://www.jockeyclub.com) records and by telephone communications with owners, trainers and referring veterinarians. These individuals were asked specific questions regarding ability to eat and drink, coughing, evidence of upper airway obstructive disease, evidence of chronic pneumonia and athletic performance. Although specific questions were asked, a standardised questionnaire was not used. Descriptive data are presented as means and medians ± s.d. and ranges.
Sixteen foals were included in the study. There were 10 colts and 6 fillies, with breed distribution of 7 Thoroughbreds, 4 Standardbreds, 3 Quarter Horse/stock horses, one Friesian and one American Saddlebred horse. Age and physical examination data and results of clinicopathological tests are listed in Table 1. Two foals were considered dysmature but term gestation, and one was premature. Two foals had serum IgG <2.0 g/l, 2 foals measured 2.0–4.0 g/l, one foal had a serum IgG 4.0–8.0 g/l, 7 foals had complete transfer of passive immunity with an IgG >8.0 g/l, and IgG was not reported for 4 foals. Twelve (75%) foals had clinical evidence of aspiration pneumonia including abnormal inspiratory and expiratory thoracic auscultation, tachypnoea, perceived dypsnoea and/or radiographic or ultrasonographic evidence of disease. Six foals (38%) had evidence of HIE (MacKay 2005). Nine of 16 foals had blood cultures submitted but none of the foals had evidence of bacteraemia. Sepsis scores were not reported for the foals. Neurological abnormalities were isolated to those associated with HIE and pharyngeal dysphagia (primarily vagal deficits). Cerebral spinal fluid samples were not collected from any of the foals. Vitamin E and selenium levels were not determined for any of the foals.
Table 1. Physical examination and clinicopathological data for foals with dysphagia due to pharyngeal dysfunction
|Respiratory rate (breaths/min)||51||48||16||24–78|
|Heart rate (beats/min)||113||120||21||84–168|
All of the foals received antimicrobials in several combinations, including ampicillind i.v. + gentamicin sulphate (GentaFuse)e i.v.; potassium penicillinf i.v. + amikacin sulphate (Amiglyde)f i.v.; ceftiofur sodium (Naxel)f i.v. or i.m.; a trimethoprim/sulphamethoxazolegper os combination; and oxytetracycline hydrochloride (Vetrimycin 100)h i.v. Five foals (31%) received no anti-inflammatory therapy. Seven foals (44%) received flunixin meglumine (Flunixiject)i i.v. and 3 of these foals also received vitamin E oiljper os. Two foals (13%) received ketoprofen (Ketofen)f i.v. and 2 foals (13%) received dexamethasone (Dexium)k i.v. Eleven foals (69%) had a nasogastric feeding tube placed for enteral nutrition. Five foals continued to nurse the mare or wore muzzles for 12–48 h before nursing was attempted, and did not receive parenteral nutrition. Four foals (25%) received supplemental partial parenteral nutrition in addition to enteral feeding; in 2 foals this was limited to supplemental dextrose.
Upper airway endoscopy was performed on all foals. The nasopharynx was described as normal based on resting examination in 4 foals, and weak, flaccid, collapsed and inflamed in 12 foals. Persistent dorsal displacement of the soft palate was observed in 2 foals but frequently displaced in one additional foal. Two foals had complete left side arytenoid paralysis in addition to inflamed, collapsing nasopharyngese. Although the arytenoids abducted, the movement was described as slow or sluggish in 2 additional foals. Guttural pouch endoscopy was not routinely performed, although milk within both guttural pouches was reported for one foal. Milk was visible in the trachea of 5 foals. Thoracic radiographs were taken in 8 foals (50%) and radiographic diagnosis in 7 of 8 cases was aspiration pneumonia based on cranio- and caudoventral alveolar and mixed bronchointerstitial pattern. Thoracic ultrasonography was performed on 12 foals (75%) and reported as normal in one foal and abnormal in 11 foals. The foal with normal thoracic ultrasonographic findings had no other signs to support a diagnosis of pneumonia. Thoracic ultrasonographic abnormalities included ventral lung field consolidation, comet tails and pleural irregularities. Auscultation over the trachea during nursing was performed in 5 foals and, in each case, a tracheal gurgle or rattling was described as the foal swallowed. No further diagnostic procedures, including CT, MRI or electromyographic studies, were performed on any of the foals.
One foal received a temporary tracheotomy and a laryngotomy was performed in one other. Both foals tolerated each procedure well and no complications with healing were reported or described by owners.
Ten of 11 foals (91%) receiving controlled enteral nutrition (nasogastric tube feeding) were transitioned to nurse the mare within a mean of 5.5 ± 4.6 days (median 4 days, range 1–14 days) with minimal to no evidence of dysphagia or aspiration. One of these foals was fed from a bucket for 3 days and then permitted to nurse from the mare. One foal made no improvement, remained dysphagic after 7 days of controlled enteral feeding, and was subjected to euthanasia. Five foals that did not receive enteral nutrition nursed successfully within 2 days (range 0–5 days). Fifteen of 16 foals (94%) were discharged alive from the hospital, nursing the mare with no evidence of dysphagia (n = 14) or mild dysphagia (n = 1), a mean of 7 ± 6 days (median = 6.3 days, range 0–22 days) after admission.
Information was available for 14 of 15 foals discharged from the hospital. This information spanned 1–5 years from hospital discharge. Thirteen foals were alive (one yearling and 12 horses >2 years old) and one was subjected to euthanasia at home 3 weeks following hospital discharge due to severe aspiration pneumonia. During hospitalisation, this foal continued to nurse from the mare, despite aspiration, at the owner's request that a nasogastric tube not be passed. Twelve of the remaining 13 horses had no evidence of chronic lower airway disease or dysphagia. Three of the 13 horses that were alive were unnamed and unraced, and are aged 2–6 years. One of these horses, a 4-year-old, was diagnosed with left recurrent laryngeal neuropathy as a neonate and had grade IV recurrent laryngeal neuropathy when re-evaluated 6 months after hospital discharge (Rakestraw et al. 1991). The second unnamed and unraced horse, a 6-year-old, had laryngeal and nasopharyngeal dysfunction and chronic pneumonia one year after hospital discharge. No long-term information regarding performance was available for the remaining 2-year-old unnamed/unraced horses. One horse, a 3-year-old, was named but is unraced. Three horses are racing and 2 are in race training. One horse is in work (dressage) and one horse is performing as a barrel racer. One horse is a pet and one stallion is used for breeding following an unsuccessful racing career.
Based on these results, dysphagia of pharyngeal dysfunction probably occurs in neonatal foals. The majority of the foals (>90%) were able to nurse successfully within 2 weeks, similar to human neonates with pharyngeal dysfunction (Gryboski 1965; Kilman and Goyal 1976). It is unclear whether the foal subjected to euthanasia in hospital would ever have recovered normal swallowing function. This foal had persistent soft palate displacement, dorsal and lateral pharyngeal wall collapse and milk within the larynx and trachea. No other cranial nerve abnormalities, other than the described presumed vagal deficits, were noted. In fact, this foal was able to suckle and had normal tongue tone. A more severe, idiopathic, congenital dysphagia related to paralysis of the constrictor muscles of the pharynx was described in children by. (Mbonda et al. 1995). Pharyngeal examination of these children showed pharyngeal and soft palate muscle paralysis with normal tongue movement and no other cranial nerve abnormalities (Mbonda et al. 1995). Children in this case series recovered normal swallowing function months to years after birth (Mbonda et al. 1995). Patients who died succumbed to tracheal aspiration, emphasising the importance of supportive care, including controlled enteral feeding and systemic antimicrobials. The cause of this more severe form of pharyngeal dysphagia is unclear. The authors theorised that it was due to central nervous system dysfunction, although no central or peripheral nerve abnormalities were found at post mortem examination in nonsurvivors (Mbonda et al. 1995).
The current study has inherent weaknesses, including its retrospective nature and incomplete diagnostic evaluation of each case. Pharyngeal dysfunction was assumed in these foals by attempting to eliminate oral and oesophageal forms of dysphagia. Fluoroscopic imaging of the swallow was not performed in any of the cases and combined with endoscopic examination of the airway, would have, provided more specific diagnostic information. A normal to strong suckle suggested normal oral function in these neonates. Foals diagnosed with megaoesophagus or oesophageal stricture, either by endoscopy or radiography, were not included, thereby minimising the inclusion of foals with oesophageal dysphagia. Foals with mechanical pharyngeal disease, such as cleft palate or palatal cyst, were also excluded. Therefore, the criteria for inclusion attempted to eliminate foals with oral and oesophageal dysphagia, leaving foals with pharyngeal dysfunction, but these methods were incomplete at best.
Foals in this study received no specific treatment for dysphagia but were supported, in general, until they could swallow successfully. Parenteral broad-spectrum antimicrobials were administered in all but one case owing to the risk and/or diagnosis of aspiration pneumonia. Indeed, one foal was subjected to euthanasia soon after hospital discharge because of the severity of its aspiration pneumonia. Controlled enteral feeding was not performed in this foal, and this highlights the importance of such a feeding regimen to minimise continued aspiration. Eleven foals were fed enterally and 5 foals were withheld from nursing and reintroduced to nursing within 12–48 h. Because these 5 foals nursed successfully within 48 h, it is possible that their degree of dysphagia was mild compared to that of the other foals. Only 2 of the 5 foals treated with feeding restriction (and no nasogastric tube placed) developed aspiration pneumonia. One of these foals was subjected to euthanasia within weeks of discharge because of pneumonia, one foal raced successfully, one is unnamed, one is named but unraced, and one is in training.
Physical therapy is attempted in human neonates with pharyngeal dysphagia by allowing the infants to suckle a pacifier, which is thought to strengthen the pharyngeal muscles (Bellmaine et al. 1972; Derkay and Schechter 1998). A similar technique might be worthy of consideration in foals with pharyngeal dysfunction, especially as enteral feeding or muzzling probably reduces spontaneous pharyngeal activity. Alternatively, milking the mare (emptying the udder) and allowing the foal to suckle for short bursts might help strengthen the pharyngeal muscles and improve coordination. A laryngotomy was performed in one foal with persistent soft palate displacement and dysphagia. This foal was able to nurse from the mare within 7 days of hospital admission and is racing successfully. The effect of the laryngotomy is unknown. However, staphylectomy via laryngotomy was performed in 2 foals to treat persistent dorsal displacement of the soft palate, and both foals were ultimately able to swallow and the soft palate returned to a normal position (Shappell et al. 1989). The effect and/or efficacy of staphylectomy or laryngotomy in foals with dysphagia due to pharyngeal dysfunction remain speculative but intriguing.
Seven of 14 foals (50%) were athletes based on race records and/or follow-up information from owners and trainers. Two nonathletic foals had evidence of recurrent laryngeal neuropathy. These 2 foals diagnosed with unilateral recurrent laryngeal nerve deficits in hospital had endoscopic evidence of left-sided disease during follow-up examinations. One of these foals also had endoscopic evidence of nasopharyngeal dysfunction but was able to swallow. Although pharyngeal function returned in the majority of foals, based on ability to swallow, recurrent laryngeal nerve dysfunction was persistent. Mbonda et al. (Mbonda, Claus, Bonnier, Evrard, Gadisseux, Lyon & 1995) reported transient paralysis of the vocal cord adductors in one infant that persisted even after the pharyngeal dysphagia resolved (Mbonda, Claus, Bonnier, Evrard, Gadisseux, Lyon & 1995). It is unclear why select vagal branch dysfunction would recover or whether the origins of each vagal neuropathy were unique.
Conflicts of interest
No conflicts of interest have been declared. None of the authors have received grants, speakers fees, or compensation from any commercial body within the past 2 years.
aBoehringer Mannheim, Mannheim, Germany.
bOlympus America, Inc., Center Valley, Pennsylvania, USA.
cBlock Scientific, Inc., Bohemia, New York, USA.
dAPP Pharmaceuticals, East Schaumburg, Illinois, USA.
eSparhawk Laboratories, Inc., Lenexa, Kansas, USA.
fPfizer, Inc. New York, New York, USA.
gQualitest Pharmaceuticals, Huntsville, Alabama, USA.
hMWI, Meridian, Idaho, USA.
iBimeda-MTC Animal Health, Inc. Cambridge, Ontario, Canada.
jNature's Bounty, Inc. Bohemia, New York, USA.
kBimeda, Inc., Le Sueur, Minnesota, USA.
Author contributions SH contributed to the study design and manuscript preparation. All authors contributed cases and reviewed the manuscript.