Dysphagia as a risk factor for sudden unexplained death in infancy

https://doi.org/10.1016/j.mehy.2006.04.028Get rights and content

Summary

The TRIAD of encephalopathy, subdural haemorrhages, and retinal haemorrhages is commonly considered diagnostic of Shaken Baby Syndrome, but the original paper describes a statistically linked QUADRAD of features, the fourth of which is a previous history of feeding difficulties (dysphagia). Recent reviews of giving pacifiers (dummies) to infants during sleeping periods have found a significant reduction in the incidence of Sudden Infant Death Syndrome. Stimulation of swallowing is a possible connection with dysphagia, which is examined here, illustrated by a well documented case.

Although amniotic fluid passes freely through the larynx of fetal mammals during fetal breathing, application of pure water to the laryngeal epithelium in infants causes choking and laryngeal closure. “Water sensors” in the surface respond to lack of chloride ions and adapt very slowly or not at all. Others have found in puppies that following application of pure water only 32% resume breathing in less than 30–40 s. The rest needed at least one saline flush, and some required artificial ventilation in addition. These receptors also respond to high potassium concentrations and acid or alkaline solutions. Normally, airway closure during swallowing or vomiting prevents entry of feed or oesophageal reflux, but in some forms of dysphagia leakage can occur, causing paroxysmal coughing, reflex laryngeal closure, and so prolonged apnoea. Recently, it has been realised that the TRIAD injuries can also result from high intracranial vascular pressures transmitted from intra-thoracic pressure surges during paroxysmal coughing, choking, etc. Triggering of such pressure surges by dysphagic accidents provides a physiological link to injuries commonly considered diagnostic of Shaken Baby Syndrome, completing the statistically identified QUADRAD of features. Further dysphagic research might reveal predictive factors, and preventative measures such as feeds of optimal pH.

Introduction

Hauck et al. [1] and Li et al. [2] have found a significant association between reduction of deaths during sleep and the provision of pacifiers (dummies). One explanation might relate to stimulation of swallowing overcoming some form of dysphagia. Obviously, dysphagic accidents can occur at any time and the study presented here relates to this more general case.

In 1993, the American Academy of Pediatrics (AAP) identified a statistical link between retinal and subdural haemorrhages, encephalopathy, occurring with no evidence of external trauma and feeding difficulties in the infant. “The infant may have a history of poor feeding, lethargy, and or irritability for days or weeks prior to the time of initial health care contact” [3]; a QUADRAD. At the time it appeared that the only mechanism by which such haemorrhages could be induced was by rapid rotational accelerations applied to the skull. This was attributed to shaking by the carer and the link to feeding was assumed to be a response by the carer to the stress of feeding difficulties, thus effectively reducing the factors to a TRIAD. Emphasis was laid on the character and the circumstances of the carer to determine why the abuse occurred and the degree of responsibility involved. Arad-Cohen et al. investigated idiopathic apparent life-threatening events (IALTE) which they defined as “…an episode that was frightening to the caretaker and that was characterised by any combination of apnea, change of color, change of muscle tone, and choking or gagging that required intervention” [4]. They found an increased rate of obstructive and mixed apnea with “near miss sudden infant death syndrome” infants compared to control subjects. In particular they found that a drop in blood oxygen saturation was significantly more prevalent when gastroesophageal reflux (GER) and apnea events appeared to be temporally associated, than with either alone. The recent recognition that similar fatal intracranial injuries could arise from raised intracranial vascular pressures transmitted from the thorax during paroxysmal coughing or effective Valsalva manoeuvres [5] and that retinopathy occurs in a wide variety accident events [6], led to this investigation of alternative explanations of this link. Illesworth [7] divided dysphagic aetiologies into gross deformity and dysfunction origins. Dysfunction was subdivided into neurological synchronisation and muscular weakness problems. A case due to muscular weakness resulting in ineffective tracheal closure during swallowing or vomiting is reported here.

An apnoeic danger arises from inappropriate stimulation of an airway protective reflex. Miller and Kiatchoosakun [8] state “ Formula or refluxate that enters the area of the hypopharynx and larynx stimulate unencapsulated unmyelinated nerve endings in the epithelium of the glottis, aryepiglottic folds and interarytenoid space. The chloride content of the offending fluid is of particular importance in activation of these receptors”. Foetuses do not choke on amniotic fluid during foetal breathing because amniotic fluid contains chloride ions. Boggs [9], studying puppies, found that pure water consistently elicited apnoea. In only 32% breathing resumed within 30–40 s. The rest required at least one saline flush for recovery and some required artificial ventilation in addition. High potassium, acid or alkaline solutions also activate these ‘water receptors’ [8]. These receptors adapt very slowly, i.e. they continue to fire for as long as they are stimulated, and only cease after the stimulating liquid is washed off, or coughed up and swallowed [9]. This reflex is reinforced by hypoxia in human infants [8]. Milk may buffer extremes of pH [10]and so be aspirated in small quantities (microaspiration) with little effect, but microaspiration of small quantities of ‘foreign’ materials may induce paroxysmal coughing, and/or upper airway closure with resulting apnoea.

Phylogenetically, the airway developed as a duct leading off the alimentary canal and this is reflected in the steep angle of its inlet, Fig. 1. The upper attachment of the inlet (aryepiglottic) sphincter is to the back of the tongue and the lower rim to tracheal structures. For satisfactory closure during swallowing or vomiting the lower rim of the inlet must rise, but the sphincter musculature (aryepiglottic, Fig. 1) is too weak to do this unaided. Safe swallowing requires various muscles to pull up the trachea, and parts of the pharynx so that there is enough “slack” for the aryepiglottic muscles to draw the airway inlet together like drawstrings on a purse, or bin-bag, and to pull the epiglottis down to cover it. In the normal infant the bolus to be swallowed is moved to the back of the tongue and trapped by the soft palate Fig. 2a. The soft palate is then raised to block off the nasal cavity, and the tongue starts to bulge backwards Fig. 2b. This action draws the hyoid bone upwards rapidly followed by raising of the hyoid and cricoid cartilages to which the upper trachea is attached. This double action can be felt by placing four fingers in line up the front of the throat and swallowing. Simultaneously, the aryepiglottic muscles hold the glottic aperture closed and pull the epiglottis down over it Fig. 2b. The vocal cords are also drawn inwards, though any fluid penetrating the aryglottic aperture during swallowing can leak through them. With further backward movement of the tongue, contraction of the various pharyngeal constrictor muscles, and relaxation of the inferior pharyngeal constrictor muscle, the bolus is rapidly transferred into the oesophagus. The tongue and soft palate then return to their normal positions, the aryglottic sphincter muscles relax and normal respiration resumes, Fig. 2c.

If the muscles are weak, Fig. 2e, the tracheal lift may be insufficient for complete aryglottic sphincter action. Also the epiglottis may be only partially lowered. If vomiting is occurring it will act as a scoop, directing reflux into the glottis. If the reflux irritates the epithelium of the glottis, vocal cords or upper trachea the oblique and transverse arytenoid muscles, Fig. 3, rotate the arytenoid cartilages to firmly appose the vocal folds, tightly sealing the upper airway, Fig. 2f.

The upper oesophageal sphincter is formed by the inferior pharyngeal constrictor muscle wrapping the oesophagus flat around the trachea, Fig. 3. Partial relaxation allows lateral ducts to form, sufficient to pass small volumes of fluids while leaving the middle region sealed [11]. Fluids then pass safely either side of the “windpipe” without passing the glottis. At weaning, lumps have to pass down the central region, and any accompanying fluid may then enter the trachea if the sphincter is not properly closed.

Gastro-oesphageal reflux (GOR) has been identified as a possible cause of SIDS [12], [13], but minor reflux through the lower oesophageal sphincter is physiological in all infants [14]. Studies using a pH probe have shown that the natural pH within the oesophagus lies between 5 and 7 [12]. Reflux into the oesophagus, but not necessarily through the upper sphincter, is marked by a drop below pH 4. This is normally restored by swallowing, and neutralised by saliva and release of bicarbonate. Increased swallowing of saliva induced by a dummy might well account for the protective effect observed during sleeping [1], [2]. The duration below pH 4 varies with the character of the last feed. Probe studies have shown that with milk feeds oesophageal pH is below 4 for only 5.1% of the time, compared to 43.8% following apple juice [12]. Reflux of low pH fluid through the upper sphincter into the pharynx, presents no respiratory hazard if the glottic sphincter is held closed until it has been re-swallowed, but if closure is defective acidic feeds may increase the risk of upper airway reflex closure following microaspiration.

Section snippets

Method

Copies were obtained of 67 written statements made to police, and some post trial comments by trial observers. Supplementary information was obtained from the mother to clarify points were necessary. From these a medical history from birth to autopsy was reconstructed and analysed.

Discussion

The fact that very small quantities of ‘foreign’ irritant solutions (iron and vitamin supplements) induced cyanotic apnoea, and even pure water induced choking shows that glottic closure was not complete. At his 6 week check up his poor head control could have been associated with prematurity, but no improvement at 4 months, points to neck muscle weakness, leaving him with a ‘leaky’ glottis.

The final incident occurred a few days into weaning. The relative’s report that the previous day his

Conclusions

It is unfortunate that the dysphagic component of the 1993 statistically identified QUADRAD of features of a mechanism of SUDI [3] has been neglected in the past, reducing the criteria to a TRIAD of features occurring around the time of death. Dysphagia, as in the case illustrated here, may not only be a very significant component of the aetiology; but ignoring it may also be masking the true aetiology of the QUADRAD originally statistically identified. Further study of the complete QUADRAD is

Declarations

There are no conflicting interests, and the work was carried out without funding support.

There was no patient experimentation so ethical approval was not involved. Data was gathered from court papers including 67 written statements made to police already in the public domain.

References (26)

  • R.S. Illingworth

    Sucking and swallowing difficulties in infants

    Arch Dis Child

    (1969)
  • D.F. Boggs et al.

    Chemical specificity of a laryngeal apneic reflex in puppies

    J Appl Physiol

    (1982)
  • H. Gray

    Splanchnology

  • Cited by (6)

    • Mimics of child abuse: Can choking explain abusive head trauma?

      2015, Journal of Forensic and Legal Medicine
      Citation Excerpt :

      Some physicians have put forward alternative explanations for findings of abusive head trauma that are said to mimic child abuse. These include choking,4 dysphagia,5 vomiting,6 rebleeding of pre-existing subdurals from birth,7 vaccinations,8 venous thrombosis,9 and others. While there are legitimate alternative explanations for some of the findings of abusive head trauma, many alternative explanations, including choking, are speculative and not scientifically supported.

    • Forensic pathoradiology of virtual autopsy

      2023, Forensic Pathoradiology of Virtual Autopsy
    • Abusive head trauma: Parenchymal injury

      2015, Diagnostic Imaging of Child Abuse
    View full text