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Saliva and the Control of Its Secretion 47
https://t.me/med1917
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Feeding and Respiration
https://t.me/med1917
Olle Ekberg, Anna I. Ha˚rdemark Cedborg, Katarina Bode´n,
Hanne Witt Hedstro¨m, Richard Kuylenstierna, Lars I. Eriksson,
and Eva Sundman
Contents
1 Introduction.............................................................. 49
2 Feeding Respiratory Pattern .................................. 50
References.......................................................................... 53
O. Ekberg (&)
Department of Diagnostic Radiology,
Skåne University Hospital, 205 02 Malmö, Sweden
e-mail: olle.ekberg@med.lu.se
A. I. Hårdemark Cedborg L. I. Eriksson E. Sundman
Department of Anaesthesiology and Intensive Care
Medicine, Karolinska University Hospital and Karolinska
Institute, Stockholm, Sweden
K. Bodén
Department of Diagnostic Radiology,
Karolinska University Hospital and Karolinska Institute,
Stockholm, Sweden
H. W. Hedström
Department of Neuroradiology, Karolinska University
Hospital and Karolinska Institute, Stockholm, Sweden
R. Kuylenstierna
Department of Otorhinolaryngology, Karolinska
University Hospital and Karolinska Institute,
Stockholm, Sweden
Abstract
Coordination of breathing and swallowing is
essential for normal bolus transportation through
the pharynx and for protection of the airways.
During passage of the bolus through the pharynx,
respiration is interrupted. Normal swallowing
occurs during the expiratory phase of breathing.
Incoordination of the feeding respiratory pattern
may lead to penetration of the bolus into the
airways. This may cause choking, death, aspiration
pneumonia, or chronic laryngitis.
1 Introduction
Swallowing and breathing are closely controlled by
specialized neuronal groups colocalized to the brainstem. Interaction occurs between neuronal groups
controlling breathing and those controlling swallowing (Dick et al. 1993; Saito et al. 2002; Ertekin and
Aydogdu 2003). Such central neuronal control, together with local anatomic conditions and sensory input
from the larynx and pharynx, allows safe and direct
passage of air, liquids, and solids. Moreover, factors
primarily thought to influence breathing (e.g., arterial
partial pressure of CO
et al. 1998; Sai et al. 2004), and other factors controlling pharyngeal function affect breathing pattern
(Nilsson et al. 1997; Hadjikoutis et al. 2000; Butler
et al. 2007; Terzi et al. 2007). Posture and positioning
are such factors.
Miller (1999), in his neurophysiological investigations of swallowing, concluded that brainstem
neuronal control is involved in the central inhibition
) affect swallowing (Nishino
2
O. Ekberg (ed.), Dysphagia, Medical Radiology. Diagnostic Imaging, DOI: 10.1007/174_2012_587,
Ó Springer-Verlag Berlin Heidelberg 2012
49
50 O. Ekberg et al.
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Fig. 1 Registrations of pharyngeal manometry, nasal air
pressure, and oral and nasal respiratory airflow by the
bidirectional gas flow discriminator, diaphragmatic and abdominal EMG, and spirometry. Recordings of two swallows at
normocapnia (a) and one swallow at hypercapnia (b). The
swallows presented show the respiratory phase pattern E–E
(inspiration–expiration–swallow–expiration). The start of pharyngeal swallowing was defined as the start of pressure rise at
the tongue base (TB-start) and the end was defined as the point
in time when the upper esophageal sphincter started to contract
of respiration during swallowing. Therefore, swallowing apnea is not an effect of closure of the vocal
folds even though, together with laryngeal closure, it
often occurs at the same time as apnea.
Swallowing apnea has also been registered in
patients after laryngectomy (Hiss et al. 2003). The
presence of swallowing apnea also remains 10 years
after laryngectomy. Therefore, swallowing apnea is a
central phenomenon and not the result of obstructive
forces of closed airways during swallowing. On the
other hand, closure of the laryngeal vestibule,
including vocal folds, is an important part of the
protective mechanism that hinders the bolus from
reaching the airways. Swallowing apnea may start
long before vocal fold closure; however, it ends when
the vocal folds begin to reopen.
(UES-start). The duration of pharyngeal swallowing is marked
with a horizontal bar (swallow). Swallowing apnea was
detected by the respiratory airflow discriminator as an oscillating signal, representing zero airflow. Diaphragmatic activity
during swallowing apnea is marked with arrows. Pharyngeal
manometry was recorded at the tongue base (TB), upper/lower
level of the pharynx (Pharynx Up./Pharynx Low.) and upper
esophageal sphincter (UES). I inspiration, E expiration. (Reprinted from Hårdemark Cedborg et al. 2009)
2 Feeding Respiratory Pattern
In a recent study, Hårdemark Cedborg et al. (2009)
explored breathing during spontaneous swallowing
using a bidirectional gas flow discriminator. They
used a complex experimental setting in volunteers
including manometry for registration of pressure at
the level of the tongue base, midpharynx, and upper
esophageal sphincter and including nasal and oral
airflow. A diaphragmatic and abdominal EMG was
used as well. Spirometry was used for quantitative
registration of airflow in liters per minute. They
studied spontaneous swallowing during normocapnia
and hypercapnia. The latter was achieved by subjects
breathing air with the addition of 5% CO
. The term
2
Feeding and Respiration 51
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Fig. 2 A swallow preceded and followed by expiration (E–E
pattern) and the diaphragmatic activity during swallowing
apnea. The time from the onset of diaphragmatic activity during
swallowing apnea to the onset of pharyngeal swallowing was
measured and is marked in the figure. The start of pharyngeal
‘‘spontaneous swallowing’’ refers to the fact that the
subjects were allowed to swallow saliva spontaneously and were not given any instruction for how to
swallow. Hypercapnia was used to evaluate how an
increased respiratory drive and higher breathing frequency interfered with spontaneous swallowing
(Fig. 1).
Hårdemark Cedborg et al. (2009) found that all
swallows occur during expiration. The normal
sequence is that expiration is interrupted by a period
of apnea, during which time the bolus passes through
the pharynx. Then the expiration is resumed. The
expiration before swallowing may be as short as
30 ms. Expiration before swallowing lasts about 1.3 s
and expiration after swallowing lasts about 1.5 s. The
preswallowing expiration time could be very short but
could always be discerned. They speculated that
swallowing is in fact controlled by the respiratory
swallowing is defined as the start of the pressure rise at the
tongue base (TB-start) and the end of pharyngeal swallowing is
defined as the start of the pressure rise at the upper esophageal
sphincter (UES-start). (Reprinted from Hårdemark Cedborg
et al. 2009)
neurons, in that sense that swallowing was only
allowed to occur during an expiratory phase. By
studying the EMG pattern, they confirmed the phrenic
nerve activity described by Saito et al. (2002). This
EMG pattern is distinctly different from that of an
inspiration and was not followed by airflow. They
called this ‘‘active breath holding.’’ This central
control of breathing ensures that respiration is stopped
before pharyngeal swallowing and that a significant
proportion (approximately 200 ml) of the tidal volume is ‘‘put on hold’’ by the activated diaphragm,
only to be expired at the end of swallowing apnea.
Expiratory airflow after swallowing clears the laryngeal inlet from misdirected bolus material, and
thereby aspiration is prevented (Fig. 2).
In an experimental prospective study, Gross et al.
(2003) showed that during a standardized puddinglike consistency swallow at three randomized lung
52 O. Ekberg et al.
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Fig. 3 Temporal
coordination of swallowing
and respiratory events in a the
upright and left decubitus
positions with normocapnia
and b the left decubitus
position with normocapnia
and with hypercapnia. All
values are in milliseconds and
are mean values ± the 95%
confidence interval. TB
tongue base, UES upper
esophageal sphincter, PhCM
middle pharyngeal
constrictor, PhCL lower
pharyngeal constrictor.
(Reprinted from Bodén et al.
2009)
Feeding and Respiration 53
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volumes (total lung capacity, functional residual
capacity, and residual volume), the pharyngeal
activity duration of deglutition for swallows produced
at residual volume was significantly longer than that
for swallows occurring at total lung capacity or at
functional residual capacity. No significant differences were found for the bolus transit time or intramuscular electromyography of the superior
constrictor. This supports the hypothesis that the
respiratory system may have a regulatory function
related to swallowing and that positive subglottic air
pressure may be important for swallowing integrity.
Hårdemark Cedborg et al. (2009) also studied the
length of preswallowing and postswallowing apnea.
The duration of swallowing apnea decreased considerably at hypercapnia. Interestingly, they found that
the duration of preswallowing apnea shortened,
whereas the duration of postswallowing apnea did not
change during hypercapnia. Hence, the temporal
positioning of pharyngeal swallowing is asymmetrical, occurring in the late part of swallowing apnea at
normocapnia but not at hypercapnia. This means that
when breathing at a high frequency the preswallowing
apnea period shortens considerably and that may put
the patient at risk of misdirected swallowing. This
may be a considerable problem in patients with
chronic obstructive pulmonary disease who have a
high respiration frequency (Martin et al. 1994;
Martin-Harris et al. 2003, 2005). Chronic aspiration
may then aggravate the patient’s pulmonary condition, introducing a vicious cycle (Gross et al. 2009).
Respiration and swallowing coordination is not
affected by changes in body position, bolus types, and
respiratory drive (Hårdemark Cedborg et al. 2010).
However, during water swallows, the duration of
preswallowing apnea is significantly longer than that
of spontaneous saliva swallow (Hårdemark Cedborg
et al. 2010). During water swallow, the duration of the
postswallowing apnea is also very constant.
Elderly adults have been shown to have a longer
swallowing apnea duration than young and middleaged adults (Hiss et al. 2001). That study also showed
that women have a longer swallowing apnea duration
than men and that the swallowing apnea duration
increases as the bolus volume increases.
Martin-Harris et al. (2005) showed a higher
occurrence of inhalation with swallowing apnea, with
increased occurrence in individuals older than
65 years. Although it was not shown, the hypothesis
is that this predisposes the elderly to aspiration
pneumonia. However, they also found that the elderly
have a prolonged swallowing apnea duration. Particularly, the onset of apnea could occur rather early
compared with the onset in young individuals.
The coordination of respiration and swallow
rhythms has also been studied in preterm and term
infants (Gewolb and Vice 2006). The initial feeding
efforts at 32–34 weeks (postmenstrual age) are characterized by periods of apneic suckle-feeding that
alternate with tidal respiration. With further development, respiration is interposed into spaces partitioned by the swallows and the breathing efforts are
integrated into an oral suck–swallow–breathing
rhythm.
It has also been shown that an increase in respiratory drive by inhalation of 7% CO
in preterm
2
infants is accompanied by a decrease in the rate of
both sucking and swallowing during nutritive feeding.
Increased ventilatory drive may directly inhibit
nutritive feeding behavior in premature infants. Also,
this speaks in favor of respiratory neurons in the
brainstem that have superior control of swallowing
and not vice versa (Timms et al. 1993).
Temporal coordination of swallowing and respiratory events has also been studied in a more global
perspective (Bodén et al. 2009; Fig. 3). This confirms
several of the studies forming the basis for the concept of a fixed pattern generator that controls
muscular activity in the swallowing apparatus
(Miller 1999).
References
Bodén K, Hårdemark Cedborg AI, Eriksson LI, Witt Hedström
H, Kuylenstierna R, Sundman E, Ekberg O (2009) Swal-
lowing and respiratory pattern in young healthy individuals
recorded with high temporal resolution. Neurogastroenterol
Motil 21:1163–e101
Butler SG, Stuart A, Pressman H, Poage G, Roche WJ (2007)
Preliminary investigation of swallowing apnea duration and
swallow/respiratory phase relationships in individuals with
cerebral vascular accident. Dysphagia 22:215–224
Dick TE, Oku Y, Romaniuk JR, Cherniack NS (1993)
Interaction between central pattern generators for breathing
and swallowing in the cat. J Physiol 465:34–44
Ertekin C, Aydogdu I (2003) Neurophysiology of swallowing.
Clin Neurophysiol 114:2226–2244
Gewolb IH, Vice FL (2006) Maturational changes in the
rhythms, patterning, and coordination of respiration and
54 O. Ekberg et al.
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swallow during feeding in preterm and term infants.
Develop Med Child Neurol 48:589–594
Gross RD, Atwood CW Jr, Grayhack JP, Shaiman S (2003)
Lung volume effects on pharyngeal swallowing physiology.
J Appl Physiol 95:2211–2217
Gross RD, Atwood CW Jr, Ross SB, Olszewski JW, Eichhorn
KA (2009) The coordination of breathing and swallowing in
chronic obstructive pulmonary disease. Am J Respir Crit
Care Med 179:559–565
Hadjikoutis S, Pickersgill TP, Dawson K, Wiles CM (2000)
Abnormal patterns of breathing during swallowing in
neurological disorders. Brain 123:1863–1873
Hiss SG, Treole K, Stuart A (2001) Effects of age, gender,
bolus volume, and trial on swallowing apnea duration and
swallow/respiratory phase relationships of normal adults.
Dysphagia 16:128–135
Hiss SG, Strauss M, Treole K, Stuart A, Boutilier S (2003)
Swallowing apnea as a function of airway closure. Dysphagia 18:293–300
Hårdemark Cedborg AI, Sundman E, Bodén K, Witt Hedström
H, Kuylenstierna R, Ekberg O, Eriksson LI (2009) Coordination of spontaneous swallowing with respiratory
airflow and diaphragmatic and abdominal muscle activity
in healthy adult humans. Exp Physiol 94:459–468
Hårdemark Cedborg AI, Bodén K, Witt Hedström H, Kuylen-
stierna R, Ekberg O, Eriksson LI, Sundman E (2010)
Breathing and swallowing in normal man––effects of
changes in body position, bolus types, and respiratory
drive. Neurogastroenterol Motil 22:1201–e316
Martin BJ, Logemann JA, Shaker R, Dodds WJ (1994)
Coordination between respiration and swallowing: respiratory phase relationships and temporal integration. J Appl
Physiol 76:714–723
Martin-Harris B, Brodsky MB, Michel Y, Ford CL, Walters B,
Heffner J (2005) Breathing and swallowing dynamics across
the adult lifespan. Arch Otolaryngol Head Neck Surg
131:762–770
Martin-Harris B, Brodsky MB, Price CC, Michel Y, Walters B
(2003) Temporal coordination of pharyngeal and laryngeal
dynamics with breathing during swallowing: single liquid
swallows. J Appl Physiol 94:1735–1743
Miller AJ (1999) The neuroscientific principles of swallowing
and dysphagia. Singular Publishing Group, San Diego,
pp 73–92
Nilsson H, Ekberg O, Bülow M, Hindfelt B (1997) Assessment
of respiration during video fluoroscopy of dysphagic
patients. Acad Radiol 4:503–507
Nishino T, Hasegawa R, Ide T, Isono S (1998) Hypercapnia
enhances the development of coughing during continuous
infusion of water into the pharynx. Am J Respir Crit Care
Med 157:815–821
Sai T, Isono S, Nishino T (2004) Effects of withdrawal of
phasic lung inflation during normocapnia and hypercapnia
on the swallowing reflex in humans. J Anesth 18:82–88
Saito Y, Ezure K, Tanaka I (2002) Swallowing-related
activities of respiratory and non-respiratory neurons in the
nucleus of solitary tract in the rat. J Physiol 540:1047–1060
Terzi N, Orlikowski D, Aegerter P, Lejaille M, Ruquet M,
Zalcman G, Fermanian C, Raphael JC, Lofaso F (2007)
Breathing–swallowing interaction in neuromuscular
patients: a physiological evaluation. Am J Respir Crit Care
Med 175:269–276
Timms BJM, DiFiore JM, Martin RJ, Miller MJ (1993)
Increased respiratory drive as an inhibitor of oral feeding
of preterm infants. J Pediatr 123:127–131
Oral and Pharyngeal Function
https://t.me/med1917
and Dysfunction
Olle Ekberg
Contents
1 Introduction.............................................................. 55
2 The Normal Swallow ............................................... 56
2.1 The Oral Stage........................................................... 56
2.2 The Pharyngeal Stage................................................ 57
2.3 The Pharyngoesophageal Segment ........................... 58
2.4 The Esophageal Stage ............................................... 59
3 The Abnormal Swallow .......................................... 59
3.1 The Oral Stage........................................................... 59
3.2 The Pharyngeal Stage................................................ 59
4 Dysfunction of the Pharyngoesophageal
Segment..................................................................... 63
5 Radiologic Evaluation in Specific Disease
Entities ...................................................................... 64
5.1 Cerebrovascular Diseases .......................................... 65
6 The Role of the Radiologist in the Design
of Therapy ................................................................ 66
References.......................................................................... 67
O. Ekberg (&)
Diagnostic Centre of Imaging and Functional Medicine,
Skåne University Hospital,
205 02 Malmö, Sweden
e-mail: olle.ekberg@med.lu.se
Abstract
Normal pharyngeal swallow is coordinated in a
precise and exact manner. It is controlled from a
swallowing centre in the brain stem. Normal
swallowing is adjusted to bolus volume tempera-
ture and viscosity. Abnormal pharyngeal swallow
may lead to misdirected swallowing that chal-
lenges the airways. Inefficient transportation into
the esophagus, stomach and bowel may lead to
dehydration and malnutrition.
1 Introduction
Normal pharyngeal swallow is precisely scheduled
and symmetric. It is finely tuned and coordinated in a
precise and exact manner to establish a safe swallow
(Miller 1986; Dodds 1989). The swallowing process
is regulated by a command center in the brainstem, a
central program generator which receives input from
the cerebral cortex and peripheral muscle and directs
the sequence of swallowing. This process is both
voluntary and involuntary and incorporates motor
activity from the oral cavity, pharynx, and esophagus.
It involves both motor and sensory activity. There is
an evolving amount of knowledge concerning normal
and abnormal swallowing (Jones and Donner 1991;
Ekberg and Wahlgren 1985; Hannig and Hannig
1987; Brühlmann 1985; Pokieser et al. 1995; Dodds
1989).
O. Ekberg (ed.), Dysphagia, Medical Radiology. Diagnostic Imaging, DOI: 10.1007/174_2011_391,
Ó Springer-Verlag Berlin Heidelberg 2012
55
56 O. Ekberg
https://t.me/med1917
Fig. 1 The oral, pharyngeal, and pharyngoesophageal segment
(PES) stages are readily appreciated radiographically. This is a
sequence of a barium swallow (a–h) in lateral projection. The
bolus is gathered in the oral cavity (a–c) and is propelled into
the pharynx by an upward and backward movement of the back
of the tongue (d)(arrow). The tilting down to a horizontal
position of the epiglottis is seen in d. The airways are closed
2 The Normal Swallow
2.1 The Oral Stage
The oral, pharyngeal, pharyngoesophageal segment
(PES), and esophageal stages of swallowing are readily
appreciated radiographically (Fig. 1). The oral stage of
swallowing is bolus-specific, i.e., the patient handles
different boluses differently,i.e., a strawberryis handled
differently from a cup of tea. Therefore, the oral stage is
notoriously more difficult to evaluate radiologically
and none of the barium reaches into the laryngeal vestibule or
trachea. The PES opens. The upward and forward movements
of the larynx including the hyoid superiorly and the PES
inferiorly are extremely important for the normal execution of
pharyngeal transit. There are no, or only minimal, remnants of
barium in the pharynx after swallowing
than the rest of the swallowing apparatus. However, the
oral stage should be included in the radiologic evaluation. The recording should start with the ingestion.
During oral processingthere is superior and inferior and
some anterior–posterior movement of the hyoid bone.
However, liquid barium should not be processed or
modified in the oral cavity. Therefore, oral preparation
for swallowing is tested with a solid or semisolid bolus.
When the ingested material is ready to be swallowed,
the material is brought onto the back of the tongue,
which obtains the shape of a groove (Hamlet et al.
1988). This is the preparatory position for swallowing.
Oral and Pharyngeal Function and Dysfunction 57
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No part of the bolus is allowed to leak anteriorly
from the mouth through the lips. Even more important
radiologically is to observe if posterior leak occurs.
The patient should be able to control the sealing of
the tongue base to the soft palate and posterior
pharyngeal wall.
2.2 The Pharyngeal Stage
The pharyngeal swallow is initiated voluntarily and
the material to be swallowed is usually called a bolus
from this point. Initiation of the pharyngeal swallow
coincides with the beginning of the anterior movement of the hyoid bone from an elevated position.
Pharyngeal constriction is probably cued by the bolus
interfering with sensory innervation at the faucial
isthmus. Radiologically it is convenient to use the
beginning of the anterior hyoid movement as the
starting point of pharyngeal swallow. The tongue then
propels the bolus posteriorly into the pharynx and
further down into the PES and cervical esophagus.
If the pharyngeal constrictor wall has normal compliance, only minor dilatation of the pharynx occurs
(Fig. 2).
The palatopharyngeal isthmus is closedby elevation
of the muscular palate and constrictor convergence,
which is most medial of the lateral walls. Normally, no
regurgitation of barium into the nasopharynx occurs.
In a patient with severe oral impairment, the pharyngeal phase may be elicited by injecting a small
barium bolus directly into the pharynx through a soft
tube. Thismay beplaced intothe pharynx via either the
mouth or the nose. Such techniques, however, are used
only for examination and not for feeding. Patients with
uncoordinated, weak, or jerky tongue movements
commonly cannot correctly position the bolus on the
tongue. Accordingly, the tongue cannot displace the
bolus posteriorly. There is a strong correlation between
an abnormal anterior movement of the hyoid bone and
overall abnormal oral and pharyngeal function, as well
as defective opening of the PES.
Protection of the airways occurs at four separable
anatomically and functionally different sites, i.e., the
vocal folds, the supraglottic portion of the laryngeal
vestibule, the subepiglottic portion of the laryngeal
vestibule, and the epiglottis (Curtis and Hudson 1983;
Curtis and Sepulveda 1983; Ekberg 1982). The most
crucial of these levels is the supraglottic portion of the
Fig. 2 An 80-year-old man with cerebrovascular disease.
There is paresis in the right side of the pharynx. This is not
seen in lateral projection (b) and is only seen in frontal
projection (a). There is pooling of contrast medium in the right
piriform sinus (broad arrow). Small amounts of barium are also
seen coating the inside of the laryngeal vestibule down to the
false vocal cords
laryngeal vestibule. Barium in the vestibule commonly extends into the trachea, as the vocal folds
offer poor protection of the lower airway (Ekberg and
Hilderfors 1985). Radiographic observation of barium
penetration into the larynx and trachea is strategic in
dysphagia evaluation. Bedside evaluation for aspiration has a low sensitivity. This is partly because many
of these patients have sensory impairment in the larynx and/or trachea and fail to cough (Splaingard et al.
1988).
Of even more fundamental importance, and
basically a prerequisite for airway closure and constrictor activity, is the elevation of the pharynx and
larynx. The airways are also protected by a movement of the thyroid cartilage toward the hyoid, and
by closure of the laryngeal vestibule. Additional
protection is offered by the epiglottis and the vocal
folds. Closure of the larynx starts at the vocal folds
and progresses in a superior direction in a peristalticlike manner.
The constrictors have a minor role in the con-
veyance of a bolus through the pharynx. The tongue
base pressure does not differ significantly between
those individuals with and those individuals without
retention (Olsson et al. 1997). This finding is
important because many research groups advocate
normal tongue-base and constrictor activity as a
prerequisite for a successful outcome of cricopharyngeal myotomy (Buchholz 1995). Tongue-base
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