GI Motility online (2006) doi:10.1038/gimo39
Published 16 May 2006
Oral, pharyngeal and esophageal motor function in aging JoAnne Robbins, Ph.D., Allison Duke Bridges, M.D. and Andrew Taylor, M.D.
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; Presbyphagia refers to age-related changes in the oropharyngeal and esophageal
swallowing of healthy adults.
; Sarcopenia is age-related loss of skeletal muscle mass, organization, and strength.
; Good health is maintained in the presence of disease-free presbyphagia.
; Healthy persons depend on a highly automated neuromuscular sensorimotor process
that coordinates chewing, swallowing, and airway protection.
; Central and peripheral nervous system changes with age affect swallowing.
; Oropharyngeal swallowing changes with healthy aging:
o Delayed onset of airway protection and upper esophageal sphincter (UES)
o Bolus adjacent to airway longer
o Reduced lingual pressures
; Esophageal swallowing changes with aging:
o Duration of esophageal peristalsis is prolonged and amplitude decreases (60–
o Esophageal contraction amplitude diminishes but function remains intact (80-
o Reduced frequency of secondary peristalsis
o Increased reflux events in elders
; Although compensatory interventions are traditional, exercise is promising to
remediate and perhaps prevent decline in function.
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Although age-related changes place older adults at risk for dysphagia, an older adult's swallow is not inherently impaired. In the 1960s the term presbyesophagus was coined for
what was thought to be deterioration in muscular structure and function within the esophagus of elderly adults. As our diagnostic methods have become increasingly sophisticated, more studies have addressed the effects of aging on normal esophageal function leading to conflicting data owing to differences in testing techniques, confounding variables including various comorbidities common in older people, and a wide range of mean age defining the elderly population. General consensus has evolved to the opinion that presbyesophagus in its original meaning does not exist but that these changes were largely a consequence of the comorbidities common in older age.
Presbyphagia refers to characteristic changes in the mechanism of oropharyngeal/esophageal swallowing of healthy older adults. Clinicians must be able to distinguish among dysphagia, presbyphagia, and other related diagnoses such as globus hystericus to avoid overdiagnosis and overtreatment of dysphagia. Older adults appear to be more vulnerable in transitioning from a healthy older swallow to experiencing dysphagia, especially with additional stressors such as acute illness or certain medications.
With the above in mind, this review discusses the normal swallow, changes related to presbyphagia, and promising management strategies for dysphagia rehabilitation in the elderly. These strategies reflect the concept that at least part of the decline in the elderly swallowing mechanism may be related to sarcopenia, the age-related loss of skeletal muscle
1mass, organization, and strength.
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The Impact of Dysphagia
It is estimated that 15% to 40% of individuals over 60 years have dysphagia. The prevalence depends on the specific populations sampled, with community-dwelling and independent
2individuals having rates near 15%. This figure is in agreement with the prevalence rates of a
number of other geriatric syndromes. Upward of 40% of people living in institutional settings,
3such as assisted living or skilled nursing facilities, are dysphagic. Based on the more
optimistic prevalence rate of 15% and the 1998 U.S. census data, it is estimated that six million adults have dysphagia. These numbers mirror the prevalence in European countries as
4well. The projected growth in the number of individuals living in skilled nursing facilities underscores the need to address dysphagia not only in ambulatory and acute care settings but also in long-term-care settings.
The consequences of dysphagia vary from social isolation owing to the embarrassment associated with choking or coughing at mealtime, to physical discomfort (e.g., food sticking in the chest), to potentially life-threatening conditions. The more ominous sequelae include dehydration, malnutrition, and both overt and silent aspiration. For the purposes of this review, aspiration is defined as the entry of material into the airway below the level of the true vocal
folds. Silent aspiration refers to the circumstance in which the bolus comprising saliva, food, liquid, or any foreign material, enters the airway below the vocal folds without triggering the
overt symptoms such as coughing or throat clearing. Both overt and silent aspiration may contribute to or result in pneumonia, exacerbation of chronic lung diseases, or even asphyxiation and death. To gain a better understanding of the impact of these consequences on an older adult and the impact of dysphagia interventions, research has aimed to develop more meaningful outcome measures. Assessments focused on pathophysiology, function, and health services are now being conducted to create more evidence-based practice in dysphagia care.
Reflecting the biomechanical nature of the normal and abnormal swallow, the precise visualization of both normal and disturbed bolus flow using videofluoroscopy has been well
5, 6detailed. This includes (1) the duration, direction, and completeness of the bolus flow; (2) the duration and extent (range) of anatomic structural movements; and (3) the relationships among bolus flow and structural movements.
Other clinical outcomes of dysphagia have become important end points to assess interventions that aim to make it possible for patients to eat and drink adequately and safely. These include measures of hydration, nutrition, and aspiration episodes. Additionally, pneumonitis, overt aspiration pneumonia, and additional forms of evidence of pulmonary damage are monitored. Nonetheless, it has been difficult to attribute mortality directly to dysphagia because it often is a secondary rather than a primary diagnosis. Top of page
In the following sections, the effects of aging on swallowing are discussed with reference specifically to the oropharynx and the esophagus. Although characteristics of normal swallowing change with age, the major constant is that normal swallowing at any age is healthy swallowing. That is, deleterious health outcomes including pneumonia, malnutrition, and dehydration are not associated with age-related swallowing changes. Good health is
maintained in the presence of disease-free presbyphagia.
Normal Oropharyngeal Swallowing
A basic understanding of the relationship between the anatomic components and functional dynamics of the normal swallowing mechanism is essential to understanding the effects of age and age-related diseases. Swallowing is an integrated neuromuscular process that consists
of a combination of volitional and relatively automatic movements. Although normal swallowing is usually conceptualized as a continuous sequence of events, the process of
6deglutition has been variously subdivided into two, three, or four phases or stages. Moreover,
the system engaged in swallowing may be divided into two basic structural subsystems:
Figure 1). This mirrors the direction of bolus flow as well as the horizontal and vertical (
7potential for gravitational influence on it.
Figure 1: Oropharyngeal swallowing mechanism.
The mechanism may be divided into two basic structural subsystems, horizontal and vertical, that mirror direction of bolus flow. (Source: Netter medical illustration used with permission
of Elsevier. All rights reserved.)
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The horizontal subsystem is largely volitional, anatomically comprising structures within the oral cavity. Within this subsystem, food is accepted, contained, and manipulated. Labial, buccal, and lingual actions, in combination with enzyme-rich intraoral fluids from salivary glands, allow manipulation of the texture of food to ultimately mechanically formulate a bolus. The cohesive bolus is moved posteriorly (and horizontally when the subject is in a normal upright seated posture) to the inlet of the superior aspect of the pharynx (Figure 2). To
accomplish this, the intrinsic and extrinsic tongue muscles change the shape and the position of the tongue, and stimulate oropharyngeal receptors that trigger ensuing portions of the
7, 8, 9swallow sequence.
Figure 2: Lateral view of bolus propulsion during swallowing.
a: Voluntary initiation of the swallow by tongue "loading." b: Bolus propulsion by tongue dorsum and UES opening anticipating bolus arrival. c: Bolus entry into the pharynx
associated with epiglottal downward tilt, hyolaryngeal excursion, and UES opening. d, e:
Linguapharyngeal contact facilitating bolus passage through (d) the pharynx and (e) the UES,
and completion of oropharyngeal swallowing. Then the entire bolus is on the esophagus. (Source: Netter medical illustration used with permission of Elsevier.)
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The pharyngeal and laryngeal components, in conjunction with the tongue dorsum, comprise the superior aspect of the vertical subsystem where gravity begins to assist in the transport of the bolus. The anatomic juxtaposition of the entrance to the airway (laryngeal vestibule) and the pharyngeal aspect of the upper digestive tract demand biomechanical precision to ensure simultaneous airway protection and bolus transfer or propulsion through the pharynx. As lingual-palatal contact sequentially moves the bolus against the posterior pharyngeal wall, the
10, 11contact contributes to the positive pressures imparted to the bolus propelling it downward.
10, 12Simultaneously, the pharyngeal constrictors begin contracting in a descending sequence,
first elevating and widening the entire pharynx to engulf the bolus (Figure 2d,e). A
descending peristaltic wave then cleanses the pharynx of residue. The tongue is the primary propulsive mechanism responsible for plunging the bolus into the vertical subsystem, but other mechanisms, such as velopharyngeal closure, also contribute to pressure gradients facilitating the bolus transfer.
Afferent nerve endings detect the sensation of a food bolus, transmitting this sensation to the swallowing center, which in turn activates vagal efferents to first relax the upper esophageal sphincter (UES) and then stimulate vagal efferents along the length of the esophagus to sequentially fire. This process triggers a peristaltic wave that consists of a circular contraction that travels distally at 2 to 4 cm/sec and transverses the entire esophagus in approximately 10 seconds. This act is termed "primary peristalsis." At the initiation of peristalsis, the lower esophageal sphincter (LES) reflexively relaxes to allow the bolus to pass into the stomach. Secondary peristalsis occurs when distention of the esophagus in the absence of oropharyngeal stimulation initiates a peristaltic wave. This wave usually begins immediately superior to the level of distention. For example, if a large food bolus is not fully cleared by
primary peristalsis, secondary peristalsis would then clear the esophagus of the bolus remnants.
In striated muscle—the oropharynx down to the mid-intrathoracic esophagus—the
coordination of peristalsis is clearly subject to control from the swallow center. In smooth muscle—the distal intrathoracic esophagus—peristalsis is likely controlled both intrinsically
as well as extrinsically. Studies have shown that vagotomy reduces the smooth muscle
13, 14segment amplitude of peristalsis but that secondary peristalsis persists. Peristalsis in the
absence of extrinsic innervation has been termed autonomous peristalsis.
The term deglutitive inhibition describes the phenomenon whereby a second swallow is
initiated before the first peristaltic contraction transverses the entire esophagus. This second swallow results in termination of the first peristaltic wave. In esophageal striated muscle, deglutitive inhibition terminates the initial peristaltic wave. If a second swallow is initiated while the first peristaltic contraction is progressing in the smooth muscle esophagus, the first wave diminishes progressively over 1 to 2 seconds.
Airway protection is ensured during the swallow by three levels of sphincteric closure: (1) aryepiglottic folds, (2) the false vocal folds, and (3) the true vocal folds. The hyolaryngeal complex is also lifted upward and forward by the combined contraction of the suprahyoid and thyrohyoid muscles, and pharyngeal elevators. This hyolaryngeal elevation and anterior movement, coupled with tongue base retraction, covers the laryngeal vestibule, diverts the bolus laterally around the airway with the epiglottis assuming a more horizontal position providing cover of the laryngeal vestibule. The biomechanical effects of hyolaryngeal excursion also, very importantly, provide the traction pull on the cricoid cartilage moving it
11, 15, 16anteriorly, an important aspect of UES opening. It must be emphasized that the UES
opening via active traction pull on the hyolaryngeal mechanism upward and forward, together with the centrally mediated neural relaxation, results in distention of the pharyngeal lumen. Timely relaxation and opening of the UES permits continuous vertical passage of the bolus
into the esophagus, and the pharyngeal transport stage of the swallow terminates when the UES returns to its hypertonic, closed "resting state."
Normal Esophageal Swallowing
When viewed in its simplest form, the esophagus is a hollow muscular tube with sphincters at each end that functions as a conduit to transport food from the oropharynx to the stomach. However, normal esophageal function involves complex interactions between the musculature of the oropharynx, the esophagus, and multiple neurologic reflexes that as yet are not fully understood.
The esophagus is an approximately 20- to 24-cm hollow muscular tube that is anatomically defined as the area between the distal portion of the UES and the proximal portion of the LES.
It is composed of an inner circular muscle layer and an outer longitudinal muscle layer. In between the two layers lies a nerve network called the myenteric plexus or Auerbach's plexus.
The esophagus comprises both striated and smooth muscle. The upper esophagus, including the UES, is composed of striated muscle. The middle esophagus contains a mixture of both smooth and striated muscle, with the proportion of smooth muscle increasing distally. The
17distal third of the esophagus and the LES exclusively contain smooth muscle.
The UES is composed of the inferior pharyngeal constrictor, the cricopharyngeus, and adjacent portions of the cervical esophagus. This complex is innervated by the pharyngeal branch of the vagus nerve. At rest, the UES is tonically contracted owing to a constant
excitatory neural discharge. The pressure of this contraction is asymmetric with higher pressures generated anteriorly and posteriorly as opposed to the lower pressures laterally. The UES pressure is increased with inspiration, Valsalva maneuver, stress, secondary peristalsis, gagging, and slow distention in the upper esophagus, and is reflexively decreased with belching, vomiting, or any mechanism that results in rapid esophageal distention. It also decreases during sleep. With oropharyngeal initiation of a swallow, the neural discharge to the UES ceases, briefly permitting UES relaxation. In its relaxed state, opening of the
sphincter is then facilitated both by the traction pull on the cricoid cartilage forward as well as by the upward hyolaryngeal mechanism. This results in a lumen through which food passes when propelled adequately by the tongue and related musculature.
Traditionally, the LES was thought to be a physiologic structure without corresponding
anatomy. However, in the late 1970s, a discrete area of asymmetrically thickened circular
18smooth muscle was identified within the diaphragmatic hiatus. The resting pressure of the
LES is between 10 and 30 mmHg greater than intragastric pressure. Unlike the UES, the
mechanism of LES resting contraction appears related to an intrinsic muscular component. Neurophysiology of Oropharyngeal Swallowing
Historically, swallowing was viewed as a sequence of reflex arcs first involving the pharynx and subsequently the esophagus. Findings from both quantitative temporospatial studies
16 in the last two decades, as well as the current knowledge of related to normal swallowing
underlying neural substrates, have provided new insights into oropharyngeal swallowing
19mechanisms showing that it is a patterned response rather than a traditional reflex.
Sensorimotor control of swallowing requires coordinated activity between both the cranial and spinal nerve systems, including the peripheral nerves, their central nuclei, and their neural centers. More specifically, the neural control of swallowing involves five major components: (1) afferent sensory fibers contained in cranial nerves, (2) cerebral and midbrain fibers that synapse with the brainstem swallowing centers, (3) paired swallowing centers in the brainstem, (4) efferent motor fibers contained in cranial nerves and the ansa cervicalis, and (5) muscle and end organs. Thus this neural network spans all levels of the neuraxis from the cerebrum superiorly to brainstem and spinal nerves inferiorly and muscles and end organs at the periphery. This relatively diffuse network is designed to integrate and sequence both the volitional and the more automatic activities of swallowing.
Healthy persons depend on a highly automated neuromuscular sensorimotor process that seamlessly coordinates the activities of chewing, swallowing, and airway protection. To accomplish a normal swallow in 2 seconds or less, the muscles of chewing interact with 26 pairs of striated pharyngeal and laryngeal muscles. The muscles involved in chewing include the masseters, temporalis, and pterygoids (all innervated by cranial nerve V); the lip and buccal musculature, the orbicularis oris, and the buccinator (all innervated by cranial nerve VII); and the intrinsic and extrinsic lingual muscles (all innervated by cranial nerve XII). Optimal structural integrity and precise neural mediation result in continuous, rapid bolus flow from the mouth to the esophagus that accommodates variation in bolus size, texture, temperature, and the individual's intent to swallow, chew, or just hold the bolus in the mouth Neurophysiology of Esophageal Swallowing
Sensory information for the entire esophagus, including both sphincters, is carried via the parasympathetic and sympathetic nervous systems. The parasympathetic involvement is via the vagus nerve whereas the sympathetic spinal afferents travel via C1 through L3 preganglions. Both networks ultimately enter the nucleus tractus solitarius (NTS), which
processes the information and activates the motor system response. These afferents also pass to higher brain centers.
Within the esophageal muscle fiber, free vagal nerve endings known as mechanoreceptors are stimulated by esophageal distention and modulate esophageal contraction. Nocireceptors, which originate through the spinal afferent pathway, respond to noxious stimuli such as acid or heat. Importantly, evidence exists that vagal afferents can modulate spinal afferents and vice versa.
Parasympathetic control through the vagus nerve regulates esophageal peristalsis. The STN activates progressive sequential firing of motor neurons that ultimately carry out the swallow response. Although the esophagus is often described as simple, Figure 3 is a diagrammatic
representation of its inherent complexities.
Figure 3: Diagrammatic representation of the intrinsic and extrinsic innervation of the esophagus.
(Source: Castell DO, ed. The Esophagus, 2nd ed. Boston: Little, Brown, 1995:17, with permission from Lippincott, Williams & Wilkins.)
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The somatic vagal efferent neurons that innervate the striated muscle portion of the esophagus including the UES originate in the medulla's nucleus ambiguus motor nuclei. The visceral motor neurons that innervate the esophageal smooth muscle, including the LES, originate in
the dorsal motor nucleus of the vagus and synapse on the myenteric plexus. Myenteric plexus neurons then directly innervate smooth muscle. Therefore, in the smooth muscle function, the myenteric plexus serves as a relay between the vagus nerve and the esophageal muscle. There are two major groups of effector neurons that innervate the smooth muscle of the esophagus. The first are excitatory neurons that mediate cholinergic contraction of circular and longitudinal muscle through muscarinic M2 and M3 receptors. The second are inhibitory nonadrenergic, noncholinergic neurons that inhibit circular muscle. There is evidence that
20nitric oxide may be the neurotransmitter responsible for inhibition effect. Many other
neuropeptides have been identified in esophageal neural tissue, although their exact roles remain unknown.
In striated muscle, efferent neurons contact nicotinic cholinergic end plates directly on muscle fibers that contain the neurotransmitters acetylcholine (ACh) and calcitonin gene-related
peptide (CGRP). Although myenteric plexi are present in areas of both smooth and striated muscle, their role in striated muscle function is unclear.
Traditional thinking suggests that causes of dysphagia are always disease related, with direct or indirect damage to effector end-organ systems of swallowing. More recent research, however, suggests that swallowing changes occur even with healthy aging. This work, focused primarily on anatomy and physiology of the oropharyngeal swallowing mechanism, describes a progression of change that may put the older population at increased risk for dysphagia. This research is particularly relevant when an older healthy adult, whose
21functional reserve (ability to adapt to stress) is naturally diminished with age, is faced with
increased stressors such as central nervous system (CNS)–altering medications, mechanical
perturbations (e.g., nasogastric tubes or tracheostomy), or chronic medical conditions (e.g., frailty) that might not elicit dysphagia in a less vulnerable individual. Translation of this work into clinical practice should provide safeguards against overdiagnosis and overtreatment of dysphagia in the elderly population.
Healthy swallowing in the elderly occurs more slowly. The increased time of swallowing in this population results from a longer horizontal component. Delays related to the vertical component also occur. In those over age 65, the initiation of laryngeal and pharyngeal events, including laryngeal vestibule closure, maximal hyolaryngeal excursion, and UES opening, are
22, 23, 24, significantly slowed relative to durations recorded in adults younger than 45 years old.25 In older healthy adults, it is not uncommon for the bolus to spend a greater length of time adjacent to an open airway, by pooling or pocketing in the pharyngeal recesses, than in younger adults. This senescent change may be associated with greater risk for airway penetration or aspiration.
Although pharyngeal events are slowed (such as delayed UES opening relative to bolus entry)
26in the elderly, the critical component of the range of UES opening is also diminished.
Scintigraphic studies have shown increased pharyngeal residue with age, possibly related to the limited UES opening, resulting in greater exposure of the laryngeal vestibule to the
27swallowed bolus in older individuals. Aspiration and airway penetration are believed to be
the most significant adverse clinical outcomes of misdirected bolus flow. In older adults, penetration of the bolus into the airway occurs more often and to a deeper and more severe
22, 28level than in younger adults.
When the swallowing mechanism is functionally altered or perturbed in older people, such as with the placement of a nasogastric tube, airway penetration can be even more pronounced. A study examining this issue found that liquid penetrated the airway significantly more
22frequently when a nasogastric tube was in place in men and women older than 70 years.
Thus, it appears that under stressful conditions or system disturbances, older individuals are less able to compensate and thus are at greater risk for airway penetration or aspiration. Age-related changes in the generation of lingual pressure also define presbyphagia. Healthy older individuals have reduced isometric tongue pressures compared with younger
29, 30individuals. In contrast, the generation of maximal lingual pressure during swallowing (which requires submaximal pressures), remains "young" in magnitude. Because the peak lingual pressures used in swallowing are lower than those generated isometrically, healthy older individuals manage to achieve pressures necessary to effect a successful swallow. The difference between maximum isometric pressure and peak swallowing pressures can be used as an indicator of the functional reserve available for swallowing. As people get older, the slower swallowing mechanics may actually be used as a benefit as it can allow greater time to recruit the necessary number of motor units for pressures critical for adequate bolus
30propulsion through the oropharynx. Thus, therapeutically speeding up an elderly patient's
swallow may be detrimental, as it may result in insufficient swallow pressures and therefore may be contraindicated as a therapy technique. This is only one of the issues that may generate experimental questions warranting study for improving treatment of dysphagia and prevention of potential untoward consequences of presbyphagia.
On occasion, the perturbations or functional alterations in the swallowing mechanism, or perhaps general age-related or disease-related frailty, may not allow safe swallows in older adults. That is, the compensation of slower swallowing may not be enough for these individuals in whom presbyphagia crosses over into dysphagia. At this point, compensatory
interventions or other rehabilitation efforts to promote safe swallowing will be required.