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