**2. Changes due to normal aging**

Swallowing is an integrated neuromuscular process in which volitional and relatively automatic movements successively are controlled. Normal swallowing consists of 5 phases: an anticipating phase, an oral preparatory phase, an oral phase, a pharyngeal phase, and finally an esophageal phase [2].

The act of swallowing starts with the anticipation when seeing and smelling the food and in a cognitively adequate elderly person with normal eyesight there are no changes whatsoever in this first phase.

In the second phase or *oral preparatory phase*, the solid bolus needs preparation to be swallowed. Of course the dentures play an important role here; elderly who are often lacking teeth or who are wearing ill-fitted dentures may experience problems in chewing and as a consequence they may have made some spontaneous adaptations as far as their diet is concerned, and they are, for example, likely to avoid raw vegetables and certain meats. It has also been established that with ill-fitted dentures the masticating muscles function less well, thereby leading to a prolongation of the chewing process and to a larger number of chewing movements [8, 9]. The saliva production, a factor strongly related to subjective comfort during swallowing, on the other hand, will remain intact with aging, with xerostomia in old age being mostly due to medication [10].

#### **2.1. Oral phase**

This phase comprises the manipulation and transportation of the food in the mouth; the tongue propels the food in one fluid movement into the pharynx. When reaching the "trigger zone" near the faucial pillars, the reflexively pharyngeal phase will be initiated. Labial, buccal, and lingual actions, in combination with saliva, all work together to manipulate the food and to ultimately mechanically formulate a bolus. This bolus is then moved to the posterior side of the mouth into the inlet of the superior aspect of the pharynx. With aging the tongue strength declines, yet during swallowing itself the tongue strength is similar as in young people probably indicating a compensation for a diminished functional reserve [11]. The duration of the oral phase increases while there is also an increase of residue in the mouth post swallowing [12]. Here, it is important to have a good evacuation of the bolus because food that rests lingering in the oral cavity may lead to bacterial overgrowth and to aspiration as well.

#### **2.2. Pharyngeal phase**

The oral cavity and pharynx contains an enormous amount of sensory receptors, represented by dense intricate nerve supply to the oral cavity, pharynx, and larynx. The exact timing of the onset of the pharyngeal swallow is triggered by reflexes based on the input from these sensory receptors in such a way that even a one-second delay in initiation can result in airway invasion of ingested material or aspiration.

reaching the lower limits of his physiological reserves, which may induce a swallowing

Swallowing is an integrated neuromuscular process in which volitional and relatively automatic movements successively are controlled. Normal swallowing consists of 5 phases: an anticipating phase, an oral preparatory phase, an oral phase, a pharyngeal phase, and finally

The act of swallowing starts with the anticipation when seeing and smelling the food and in a cognitively adequate elderly person with normal eyesight there are no changes whatsoever

In the second phase or *oral preparatory phase*, the solid bolus needs preparation to be swallowed. Of course the dentures play an important role here; elderly who are often lacking teeth or who are wearing ill-fitted dentures may experience problems in chewing and as a consequence they may have made some spontaneous adaptations as far as their diet is concerned, and they are, for example, likely to avoid raw vegetables and certain meats. It has also been established that with ill-fitted dentures the masticating muscles function less well, thereby leading to a prolongation of the chewing process and to a larger number of chewing movements [8, 9]. The saliva production, a factor strongly related to subjective comfort during swallowing, on the other hand, will remain intact with aging, with xerostomia in old age being mostly due to

This phase comprises the manipulation and transportation of the food in the mouth; the tongue propels the food in one fluid movement into the pharynx. When reaching the "trigger zone" near the faucial pillars, the reflexively pharyngeal phase will be initiated. Labial, buccal, and lingual actions, in combination with saliva, all work together to manipulate the food and to ultimately mechanically formulate a bolus. This bolus is then moved to the posterior side of the mouth into the inlet of the superior aspect of the pharynx. With aging the tongue strength declines, yet during swallowing itself the tongue strength is similar as in young people probably indicating a compensation for a diminished functional reserve [11]. The duration of the oral phase increases while there is also an increase of residue in the mouth post swallowing [12]. Here, it is important to have a good evacuation of the bolus because food that rests lingering in the oral cavity may lead to bacterial overgrowth and to aspiration as well.

The oral cavity and pharynx contains an enormous amount of sensory receptors, represented by dense intricate nerve supply to the oral cavity, pharynx, and larynx. The exact timing of the onset of the pharyngeal swallow is triggered by reflexes based on the input from these sensory

problem.

56 Seminars in Dysphagia

**2. Changes due to normal aging**

an esophageal phase [2].

in this first phase.

medication [10].

**2.1. Oral phase**

**2.2. Pharyngeal phase**

This phase starts with the initiation of the swallowing reflex, and the triggering of this reflex is somewhat delayed in the elderly [13], which again points to a reduced functional reserve although there is still sufficient time to close the airway.

In the elderly, there is an increased distance between the hyoid bone and the larynx [14, 15]. This leads in combination with sarcopenia to a larger pharyngeal space that needs clearing at deglutition [14]. The hyoidal movement in the superior and anterior direction plays a crucial role as it is important not only for safety reasons as it moves the entrance of the airway further away from the bolus but also for reasons of efficiency as this movement is responsible for the opening of the upper esophageal sphincter (UES). This movement declines with aging and is even in healthy elderly already significantly reduced compared with younger individuals.

The safety of swallowing is further bolstered by the movement of the epiglottis and by active approximation of the vocal cords and both mechanisms remain intact [16, 17].

The opening of the UES, as observed on videofluoroscopy, is unchanged but in approximately 30% of the healthy elderly one can observe the presence of a so-called cricopharyngeal bar, a posterior impression at the pharyngoesophageal segment [15]. The cricopharyngeal bar is a frequent incidental radiologic finding, which in many cases does not cause any symptoms.

When the UES is investigated in the elderly with manometry, it shows a decreased relaxation of the UES often in combination with increased amplitude of the pharyngeal contraction [2, 18-22]. The intrabolus pressure measured at the level of the UES is also elevated. And to be complete in the description of this phase we see that at the top of the pharynx the velophar‐ yngeal closure remains intact.

Due to these physiological changes normal in aging, the pharyngeal transit time is significantly increased in old age [2].

Swallow safety and swallow efficiency not only imply an adequate motor function but also a preserved sensibility. Increasing age is often associated with a declined perception of spatial tactile recognition on the lip and tongue [23] and the rest of the oral cavity.

A study that used air pulses at the posterior pharyngeal wall at the level of the piriform sinuses showed a decreased sensibility in old age and as a consequence the amount of pharyngeal residue required to initiate a so-called clearing swallow proved to be significantly higher than in young persons [24-26].

In older healthy adults, it is not uncommon for the bolus to spend a greater length of time next to an open airway, by pooling in the piriform sinuses and in the valleculae, than in younger adults. This senescent change may be associated with greater risk for airway penetration or aspiration.

Swallow safety means that no material enters the airway; one distinguishes between penetra‐ tion and aspiration. While in penetration nothing descends beyond the level of the true vocal cords, one speaks of aspiration when this is indeed the case with material ending up in the tracheal structures. In healthy elderly, there seems to be an increased incidence of penetration but not of aspiration [2, 27]. Another important clinical parameter consists of swallow efficiency, that is, the possibility to transport a bolus through the pharynx without leaving residue. Several studies have shown that residue both at the vallecular and the piriform sinuses level is frequently encountered in healthy asymptomatic elderly [22, 28]. With a new technique (Automated Impedance Manometry or AIM), it is possible to measure a Swallow Risk Index (SRI) [22]. This index is based on a number of manometric and impedance parameters and is clearly higher in the elderly pointing at an elevated level of swallowing dysfunction.

#### **2.3. The esophageal phase**

In 1974, it was shown that in elderly men above 80 years of age without comorbidities the peristaltic amplitude was significantly lower than in younger controls, but without changes in the speed or duration of the peristaltic wave [29]. The authors stated that aging results in a weaker esophageal muscle but with intact innervation. Later on the technique to perform manometric studies was further improved facilitating the discovery that the duration of the peristaltic wave increases in the aged population [30, 31].

Another manometric study of healthy Japanese volunteers showed that the elderly population (>60 years) had decreased peristaltic contraction amplitude compared to the young control group (<49 years) [32]. But in a similarly large study comparing older (>65 years) and younger (<45 years) patients with dysphagia, they could not find any significant difference in peristaltic amplitude, duration, and LES (lower esophageal sphincter) pressure [33].

Finally several studies have indicated an increase in both the amount of failed peristaltic events as well as in synchronous contractions [34].

To summarize, most studies in healthy elderly indicated that approximately 90% of these subjects had impaired peristaltic activity, while no peristalsis at all was observed in one third of them. Moreover the incidence of non-peristaltic contractions of the esophagus increases with age.

In conclusion, it is not easy to compare the preceding studies due to differences in subject population, average ages, and degree of comorbidities as well as differences in manometric and radiographic techniques. It appears that in subjects older than 90, the majority have comorbidities that would possibly predispose them to an esophageal motility disorder making it difficult to distinguish whether dysmotility in this group is due to age and disease or disease alone. In subjects aged 60 to 80, the duration of peristalsis is prolonged and the amplitude may be lessened, although whether these findings are clinically significant remains unclear. In healthy subjects aged from 80 to 90, esophageal muscle weakness exists but the swallow function remains intact. Although certain parameters change significantly with aging, the swallow safety and swallow efficiency are still adequately preserved in normal aging.

A summary of the changes can be found in Table 1.


cords, one speaks of aspiration when this is indeed the case with material ending up in the tracheal structures. In healthy elderly, there seems to be an increased incidence of penetration but not of aspiration [2, 27]. Another important clinical parameter consists of swallow efficiency, that is, the possibility to transport a bolus through the pharynx without leaving residue. Several studies have shown that residue both at the vallecular and the piriform sinuses level is frequently encountered in healthy asymptomatic elderly [22, 28]. With a new technique (Automated Impedance Manometry or AIM), it is possible to measure a Swallow Risk Index (SRI) [22]. This index is based on a number of manometric and impedance parameters and is

clearly higher in the elderly pointing at an elevated level of swallowing dysfunction.

peristaltic wave increases in the aged population [30, 31].

as well as in synchronous contractions [34].

A summary of the changes can be found in Table 1.

age.

amplitude, duration, and LES (lower esophageal sphincter) pressure [33].

In 1974, it was shown that in elderly men above 80 years of age without comorbidities the peristaltic amplitude was significantly lower than in younger controls, but without changes in the speed or duration of the peristaltic wave [29]. The authors stated that aging results in a weaker esophageal muscle but with intact innervation. Later on the technique to perform manometric studies was further improved facilitating the discovery that the duration of the

Another manometric study of healthy Japanese volunteers showed that the elderly population (>60 years) had decreased peristaltic contraction amplitude compared to the young control group (<49 years) [32]. But in a similarly large study comparing older (>65 years) and younger (<45 years) patients with dysphagia, they could not find any significant difference in peristaltic

Finally several studies have indicated an increase in both the amount of failed peristaltic events

To summarize, most studies in healthy elderly indicated that approximately 90% of these subjects had impaired peristaltic activity, while no peristalsis at all was observed in one third of them. Moreover the incidence of non-peristaltic contractions of the esophagus increases with

In conclusion, it is not easy to compare the preceding studies due to differences in subject population, average ages, and degree of comorbidities as well as differences in manometric and radiographic techniques. It appears that in subjects older than 90, the majority have comorbidities that would possibly predispose them to an esophageal motility disorder making it difficult to distinguish whether dysmotility in this group is due to age and disease or disease alone. In subjects aged 60 to 80, the duration of peristalsis is prolonged and the amplitude may be lessened, although whether these findings are clinically significant remains unclear. In healthy subjects aged from 80 to 90, esophageal muscle weakness exists but the swallow function remains intact. Although certain parameters change significantly with aging, the swallow safety and swallow efficiency are still adequately preserved in normal aging.

**2.3. The esophageal phase**

58 Seminars in Dysphagia
