1. science
2. medicine
3. surgery

Articles in PresS. J Appl Physiol (November 6, 2014). doi:10.1152/japplphysiol.00276.2014
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Physiology in Medicine: Physiological Basis of Diaphragmatic Dysfunction with
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Abdominal Hernias - Implications for Therapy
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Patrick Koo
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Eric J. Gartman
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Jigme M. Sethi
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F. Dennis McCool
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Address correspondence to
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F. Dennis McCool, MD
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Alpert Medical School of Brown University
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Memorial Hospital of Rhode Island
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Division of Pulmonary, Critical Care, and Sleep
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111 Brewster Street, Third floor
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Pawtucket, Rhode Island 02860
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Fax: (401) 729-2606
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Office: (401) 729-2635
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Running head: Interaction of Abdominal Hernias on Diaphragm Function
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All authors have no conflict of interests to disclose.
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Copyright © 2014 by the American Physiological Society.
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Abstract
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An incisional hernia is a common complication after abdominal surgery. Complaints of
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dyspnea in this population may be attributed to cardiopulmonary dysfunction or
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deconditioning. Large abdominal incisional hernias, however, may cause diaphragm
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dysfunction and result in dyspnea, which is more pronounced when standing (platypnea).
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The use of an abdominal binder may alleviate platypnea in this population. We discuss
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the link between diaphragm dysfunction and the lack of abdominal wall integrity, and
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how abdominal wall support partially restores diaphragm function.
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Keywords: platypnea, abdominal hernia, diaphragm dysfunction, ultrasound
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Introduction
Platypnea is defined as shortness of breath that worsens when standing. It is
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usually attributed to conditions which cause oxyhemoglobin desaturation when standing
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(orthodeoxia), such as anatomic cardiovascular defects causing right-to-left shunts,
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vascular anomalies seen with hepato-pulmonary syndrome (17), pulmonary arterio-
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venous malformations (9), or patent foramen ovale (4, 18). Typically, diaphragm
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dysfunction is associated with orthopnea, not platypnea. However, the lack of abdominal
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wall integrity may result in diaphragm dysfunction and platypnea. An intact abdominal
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wall is a needed to enhance diaphragm function by optimizing pre-contraction diaphragm
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length and configuration and by allowing for a more effective increase in abdominal
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pressure when the diaphragm contracts (7). Respiratory dysfunction has been well
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described in infants with congenital abdominal wall defects (5). However, this
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phenomenon is not well appreciated in adults with abdominal wall anomalies.
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The development of a ventral hernia is a relatively common complication of
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abdominal surgery. If large enough, a ventral abdominal hernia may lead to diaphragm
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dysfunction accompanied by complaints of dyspnea and/or platypnea. These symptoms
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are often inadvertently attributed to factors such as deconditioning or atelectasis rather
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than diaphragm dysfunction. The purpose of this manuscript is to heighten awareness of
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diaphragm dysfunction as a complication of large ventral hernias and as a cause of
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dyspnea in this patient population. We will address how a compromised abdominal wall
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leads to diaphragm dysfunction, why the standing position predisposes to diaphragm
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dysfunction in this patient population, and how the use of an abdominal binder or
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definitive surgical repair ameliorates symptoms of dyspnea.
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Diaphragm Dysfunction and Abdominal Wall Integrity
The abdomen is an essential component of the respiratory pump. It consists of
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incompressible (fluid-like) abdominal contents (19) and the structures that encase these
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contents, namely the pelvic floor, spine, paraspinal muscles, and the anterior abdominal
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wall. Of these structures, only the anterior abdominal wall is distensible. The lack of
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support of the abdominal contents by the anterior abdominal wall results in outward
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bulging of the abdominal wall when standing. This shift of support of abdominal
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contents from the diaphragm to the bulging anterior abdominal wall impairs diaphragm
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function by 1) shortening the diaphragm, 2) reducing its mechanical advantage, and 3)
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impairing diaphragm force-velocity properties.
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When abdominal compliance is abnormally high, as with a flaccid abdominal wall
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due to a large ventral hernia, the abdominal contents shift outward through the ventral
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hernia, and gravitational forces pull the diaphragm caudally. (Figure 1) Consequently,
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end-expiratory lung volume (EELV) is increased; the diaphragm is shortened; and it
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becomes “weaker” due to alterations in its length-tension properties. EELV may increase
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by as much as 700 mL, (Figure 2) an increase in volume sufficient to reduce diaphragm
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strength and endurance, thereby predisposing it to fatigue. (20) These adverse effects of
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the standing posture on diaphragm length are ameliorated by assuming the seated or
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supine position, where the abdominal contents shift cephalad and lengthen the diaphragm
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(Figure 1). Independent of the above gravitational effects, the presence of a large
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abdominal hernia compromises the insertional actions of the abdominal wall muscles on
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the lower rib cage. Normally, abdominal wall muscles act to configure the lower rib cage
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in a fashion that optimizes diaphragm pre-contraction length (15). This beneficial effect
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of abdominal wall muscle activity on diaphragm configuration also is absent in infants
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with congenital abdominal wall defects.
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The conversion of diaphragm tension to transdiaphragmatic pressure (Pdi) is
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dependent on diaphragm mechanical advantage. The abdominal wall muscles act to
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improve diaphragm mechanical advantage by reducing the anteroposterior and transverse
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diameters of the lower rib cage. This action improves mechanical advantage by 1)
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making the angle of diaphragm insertion into the lower rib cage more acute, thereby
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directing more tension caudally; 2) reducing the area of the abdomen spanned by the
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diaphragm; and 3) increasing the length of the zone of apposition. According to the
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“piston in cylinder” model of mechanical advantage, the smaller the surface area spanned
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by the diaphragm, the greater the pressure developed for a given tension (Figure 3). The
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mechanical action of the diaphragm on the lower rib cage also is compromised because
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the length of the zone of apposition is reduced when standing due to the shift of
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abdominal contents caudally to the flaccid abdominal wall. Normally, as the diaphragm
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contracts, the increase in abdominal pressure is transmitted through the zone of
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apposition and expands the lower rib cage. When the length of the zone of apposition is
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decreased, the inflationary action of the diaphragm on the lower rib cage is reduced. In
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the supine position, the abdominal contents push the diaphragm cephalad, increase the
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length of the zone of apposition, decrease the radius of diaphragmatic curvature, and
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restore the fulcrum effect of the abdomen on diaphragmatic contraction.
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There is an inverse relationship between skeletal muscle force and velocity of
contraction for a given neural stimulus. An intact abdominal compartment is essential for
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the diaphragm to operate with a stable force-velocity relationship. The contents of the
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abdomen impede diaphragm descent, thereby slowing diaphragm shortening velocity and
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increasing diaphragm force for a given degree of neural stimulus. In the presence of a
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large ventral hernia, the abdomen provides less impedance to caudal movement of the
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contracting diaphragm. Consequently, the diaphragm will contract with greater velocity
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and less force, and neural drive will have to be increased to generate the requisite
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pressure to inflate the lung. This altered force-velocity characteristic combined with an
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increase in EELV due to the highly compliant abdominal wall, alterations in pre-
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contraction diaphragm geometry, and impaired mechanical advantage will predispose the
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diaphragm to fatigue when the individual with a large hernia assumes the standing
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position. (11) The improvement in diaphragm function in the supine or seated positions is
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likely related to shifting support of the abdominal contents from the anterior abdominal
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wall to the back and side walls of the abdominal cavity, thereby ameliorating the adverse
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effects due to gravitational shifts of abdominal contents related to the abdominal wall
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hernia.
In summary, a flaccid abdominal wall results in a shift of abdominal contents
caudally and anteriorly when an individual with an abdominal wall hernia stands.
This shift in contents impacts diaphragm performance by causing it to operate over
shorter length, higher velocities, and impaired mechanical advantage. These factors
reduce diaphragm strength and predispose it to fatigue. The impact of these factors is
most prominent when the individual is standing and may lead to diaphragm fatigue
and platypnea. (Figure 4)
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Assessment of Diaphragm Dysfunction
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The initial evaluation of diaphragm dysfunction includes measuring lung
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volumes, seated and supine vital capacities (VC), and maximum inspiratory (MIP) and
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expiratory (MEP) pressures. Typically, diaphragm dysfunction results in a reduction in
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VC and MIP. MEP may be preserved when the disorder causing diaphragm dysfunction
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involves solely the phrenic nerve or the diaphragm itself, in which case the contractile
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ability of the abdominal muscles is preserved. When an individual with diaphragm
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dysfunction lies supine, VC may be further reduced by 20 to 50% when compared to
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seated measures of VC. However, with a large abdominal hernia, measurements of
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standing VC may be reduced, whereas measures of seated and supine VC may be normal
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(Table 1). This is explained by the increase in functional residual capacity (FRC), which
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changes diaphragm length, weakens the diaphragm, and reduces total lung capacity
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(TLC). Thus, the reduction in VC is primarily attributed to the reduction in TLC.
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Further evaluation of the diaphragm may include fluoroscopy, measurements of
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transdiaphragmatic pressure, or diaphragm ultrasonography. Imaging the diaphragm in
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the zone of apposition using ultrasound is an application which is increasingly used to
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identify diaphragm dysfunction. Diaphragm ultrasonography is easily learned, is readily
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available for bedside exams, and can be performed with the patient seated, supine or
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standing. With this technique, diaphragm thickness (tdi) is measured at end-expiration
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and end-inspiration. A lack of diaphragm thickening during inspiration (∆tdi) is
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diagnostic of diaphragm dysfunction. Figure 5 depicts diaphragm ultrasound images of a
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patient with a large abdominal hernia in the seated and standing positions. When the
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individual stands, initially the diaphragm contracts normally. However, after two to three
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minutes, the diaphragm no longer thickens and paradoxically becomes thinner with
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inspiration, indicating loss of diaphragm contribution to tidal breathing. At the same
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time, the patient developed a rapid shallow breathing pattern and paradoxical motion of
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the abdominal wall inward during inspiration, findings consistent with diaphragm
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dysfunction. In the seated position, ultrasonography revealed that both hemidiaphragms
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thicken appropriately during inspiration.
In summary, diaphragm dysfunction in patients with abdominal wall hernias occurs
with the patient in the standing rather than supine position. It can be suspected when
the patient complains of platypnea and standing VC is reduced when compared to
seated or supine measure of VC. The diagnosis of diaphragm dysfunction can be
confirmed using ultrasound as the absence of diaphragm contraction (thickening).
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Compensatory Breathing Strategies with Abdominal Wall Hernia
The strategy most commonly used to compensate for diaphragm dysfunction is to
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recruit the inspiratory “rib cage” muscles to lift the rib cage and increase lung volume.
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Individuals with large abdominal hernias who adopt this strategy exhibit paradoxical
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inward motion of the anterior abdominal wall, (Figure 6) negative values for
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transdiaphragmatic pressure (3), and no thickening (contraction) or paradoxical thinning
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of the diaphragm during inspiration (Figure 1). Alternatively, the abdominal muscles
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may be actively recruited to lower lung volume below FRC. When the abdominal
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muscles relax at end-expiration, passive inspiration ensues due to the outward recoil of
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the chest wall. Individuals with large ventral hernias are unable to effectively use this
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strategy because of the lack of abdominal muscle integrity.
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The use of rib cage muscles to inhale reduces the load placed on the diaphragm
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and lessens the likelihood that the diaphragm will fatigue. When standing, initially the
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diaphragm contracts normally. However, this comes at a cost of increased energy
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expenditure due to the diaphragm operating over shorter lengths and at greater velocities,
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which causes tachypnea and shortness of breath. After several minutes, the diaphragm
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will fatigue and inspiration becomes dependent on use of the accessory rib cage muscles.
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The lack of diaphragm contraction and thickening after 2-3 minutes in the standing
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position and development on platypnea is consistent with this mechanism.
In summary, individuals with abdominal wall anomalies are limited to using the
inspiratory muscles of the rib cage to compensate for a weak or ineffective
diaphragm. The rib cage muscles are used to assist with ventilation but are weaker
than the diaphragm. When fatigue ensues, platypnea develops.
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Management Options
Application of an abdominal binder or surgical repair may improve diaphragm
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function in patients with a large abdominal wall defect (Figure 7). Support of the
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abdominal contents is enhanced when an abdominal binder is placed under the lower rib
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cage or when the abdomen is submerged in water. With a binder in place or when water
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encases the abdominal wall, the abdominal contents will shift towards the diaphragm,
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optimize its configuration for contraction, and slow its velocity of shortening. Individuals
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with cervical spinal cord injuries similarly have flaccid abdominal walls due to lack of
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spinal innervation. An abdominal binder has been shown to increase maximal inspiratory
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and sniff pressures, vital capacity, forced expiratory volume over one second (FEV1), and
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peak expiratory flow rate in this population by (8, 13, 21). This enhancement of
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pulmonary function is likely due to improved diaphragm function. There are no
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published, prospective data to support the use of an abdominal binder for patients who
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are symptomatic from incisional hernias. However, Celli et al (3) published a report of a
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patient who demonstrated improvement in diaphragm function and platypnea after
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application of an abdominal binder. By contrast, providing more support of the
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abdominal wall in patients with bilateral diaphragm paralysis will worsen respiratory
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function because the increase in subdiaphragmatic pressure pushes the flaccid diaphragm
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into the thoracic cavity (12).
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An incisional hernia is a common complication following abdominal surgery with
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the incidence ranging from 9 to 20 percent (6). Symptoms of dyspnea in these patients
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may be attributed to cardiopulmonary dysfunction rather than a dysfunctional abdominal
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wall. The ease of repair of an abdominal wall hernia is dependent on its size, the type of
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herniated viscera, the duration of the hernia, and history of previous episodes of bowel
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strangulation and obstruction. Small incisional hernias (< 5 cm) are relatively easy to
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treat compared to larger hernias. Indications for surgical repair are typically based on
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balancing the potential risk of bowel strangulation and obstruction with the risk of
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surgical complications (1, 2, 16). A Danish study examined the early and late outcomes
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after elective incisional hernia repair (10). From a target population of 3,258 patients, the
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30-day readmission, reoperation, and mortality rates were 13.3%, 2.2%, and 0.5%,
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respectively. About 10% of those who underwent hernia repair had recurrence and
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required reoperation. Readmission and reoperation rates were the highest with open
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repair compared to laparoscopic repair and with large hernia defects up to 20 cm.
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In theory, surgical reduction of the incisional hernia should alleviate respiratory
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symptoms. Unfortunately, data are lacking regarding the repair of hernias and resolution
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of respiratory symptoms. Therefore, we do not have guidance on when to refer for
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surgical repair of a large abdominal hernia based on the severity of respiratory symptoms.
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Given that surgical repair may provide potential respiratory benefits, symptomatic
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patients should consider exploring the surgical option. However, the recurrence rate
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requiring reoperation after the index repair is high, especially in patients with large
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defects. A multidisciplinary approach with detailed discussion between the patient,
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surgeon, primary care provider, and other medical subspecialties should be considered
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when contemplating the risks and benefits of the procedure. In the previously mentioned
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patient example, the individual decided to undergo surgical repair of a large abdominal
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hernia after a lengthy discussion about risks with her surgeon and pulmonologist. Six
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months after surgical abdominal hernia reduction with mesh placement, she demonstrated
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marked improvement in dyspnea and platypnea, resumption of normal diaphragmatic
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thickening when standing, and she is now able to perform her daily activities without
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limitations.
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In summary, increasing support of the abdominal contents by the application of an
abdominal binder will ameliorate complaints of dyspnea in patients with abdominal
wall hernias. Application of an abdominal binder reduces and shifts the abdominal
contents toward the diaphragm, moving it to an optimal configuration for
contraction. The use of abdominal binders should be considered initially since they
are non-invasive. Surgical repair provides another option to decrease abdominal
wall compliance. It may be beneficial for those who do not improve with noninvasive management, but due to a paucity of available data, guidance is lacking for
when to refer symptomatic patients for surgical repair.
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Summary
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An intact abdominal wall is necessary for optimal diaphragm function. With large
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ventral hernias, the abdominal contents are not well supported by the anterior abdominal
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wall. Consequently, the diaphragm is displaced caudally and EELV increases. The
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diaphragm becomes shorter; the zone of apposition is reduced; mechanical advantage is
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impaired; the diaphragm contracts with greater velocity; and it is more prone to fatigue
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due to reduced force generation and increased shortening velocity. These problems
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become evident when the patient stands and platypnea ensues. Studies evaluating the use
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of an abdominal binder and hernia repair surgery to manage respiratory symptoms are
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lacking, and they are needed to assess these potential options for improving respiratory
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function in patients with a large incisional hernia.
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References
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8. Goldman JM, Rose LS, Williams SJ, Silver JR, Denison DM. Effect of abdominal
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endurance of inspiratory muscles. J Appl Physiol 1986;60(1):299-303.
12. McCool FD, Mead J. Dyspnea on immersion: mechanisms in patients with bilateral
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14. McCool FD, Wang J, Ebi KL. Tidal volume and respiratory timing derived from a
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Figure Legends
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Figure 1. Schematic depicting the change in diaphragm position in a normal individual
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and in an individual with an abdominal hernia in the standing and supine positions. When
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an individual with an abdominal hernia stands, gravity displaces the abdominal contents
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caudally and ventrally. There is more pronounce caudal diaphragm displacement in the
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individual with the abdominal wall hernia than in the normal. In the supine position, the
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abdominal contents move inward and push the diaphragm cephalad.
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Figure 2. Change in EELV estimated using magnetometry. EELV increases by
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approximately 700 ml when the patient stands indicating that the diaphragm is operating
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over shorter lengths in this position.
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Figure 3. Schematic of the “piston in cylinder” model of mechanical advantage applied to
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the diaphragm. A) The zone of apposition is the part of the diaphragm, which lies against
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the lower rib cage. The area of the cylinder is the area projected by the diaphragm dome
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in the zone of apposition. B) Pressure is defined as force/area. As one applies force in a
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downward direction, the pressure in the cylinder is lowered. If the diaphragm is operating
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at higher lung volumes, the area of the cylinder is increased and pressure is reduced for a
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given force.
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Figure 4. Schematic illustrating the interaction between the abdominal wall and
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diaphragm function. A highly compliant abdominal wall interferes with normal
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diaphragm function as depicted on the right column.
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Figure 5. Diaphragm ultrasound images obtained in the seating and standing positions.
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The red arrows indicate the borders of the diaphragm muscle (pleura and peritoneum) at
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the zone of apposition. The red line indicates the thickness of the diaphragm.
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Figure 6. Rib cage and abdominal dimensions were assessed with magnetometers with
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the patient (A) seated, (B) standing without an abdominal binder and (C) standing with an
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abdominal binder. When seated, the rib cage and abdominal movements are synchronous
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(as marked by a vertical line). In the standing position without the binder, the rib cage
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excursion is greater, and there is paradoxical inward movement of the abdomen with
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inspiration. With application of an abdominal binder, the rib cage and abdominal motion
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is more synchronous.
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Figure 7. The optimal diaphragm force-velocity relationship is depicted as the upper line
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(seated position). When an individual with an abdominal hernia stands, the displacement
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of the abdominal contents causes the diaphragm to move caudally, shortening the
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diaphragm (arrow 1). The diaphragm generates reduced tension. The loss of impedance
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from displacement of the abdominal contents causes the diaphragm to contract with
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increased velocity further reducing force (arrow 2). When the diaphragm fatigues, the
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accessory inspiratory muscles are recruited to increase force generation (arrow 3).
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Fatigue and platypnea ensue. Application of an abdominal binder or surgical repair of the
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abdominal hernia potentially reduces abdominal compliance and shifts the diaphragm
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back to the optimal force-velocity configuration (thick red arrow).
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Table 1: Vital Capacity in the seated, supine and standing positions; and seated maximum
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expiratory pressure (MEP) and maximum inspiratory pressure (MIP)
Units
Seated %
Supine
Supine %
% change
Standing
% change
actual
predicted
actual
predicted
Supine
actual
standing
2.29
84
Units
Actual
% Predicted
MEP
cm H2O
-42
59
MIP
cm H2O
-46
50
SVC
L, btps
Seated
2.25
83
-2
1.85
-20
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Vital capacity (VC) performed in the seated and supine positions. No change in VC was
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observed between the seated and supine positions. VC was reduced by 20% between the
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seated and standing position. Both MEP and MIP were reduced.
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Abdominal Wall Hernia and Diaphragm Position
Standing
Normal
Abdominal
Hernia
Supine
Positional Change in End-Expiratory Lung Volume (Tidal Breathing)
Seated
2L
Calculated Volume (L)
Transition
to
Standing
Standing
Increasing end-expiratory
lung volume
Seated
Talking
End-Expiratory Lung Volume
Time (90-second interval)
“Piston in Cylinder” Model of Mechanical Advantage
Interaction Between the Diaphragm and Abdominal Wall
Abdominal Wall
Ventral Hernia
High Compliance
No Hernia
Normal Compliance
Caudal Shift of
Diaphragm
Minimized by Intact
Abdominal Wall
Normal
Impedance
Slows
Diaphragm
Shortening
Velocity
↑ Pressure
Generation
Minimal
↑EELV
↑↑↑ Caudal Shift of
Diaphragm
When standing
↑EELV
↓ Lower Rib Cage
Expansion
Near Optimal
Diaphragm
Length
↓Diaphragm
Length
↑ Pressure
Generation
↓ Pressure
Generation
Asymptomatic
↓Length of the
Zone of Apposition
Impaired Mechanical
Advantage
↓Pressure Generation
↑Breathing Frequency and Platypnea
↓Impedance
leads to
↑Diaphragm
Shortening
Velocity
↓ Pressure
Generation
Chest Wall Motion With Abdominal Hernia
4010
4010
4000
4000
3990
3990
3980
3980
3970
3970
3960
3960
Signal Strength
Signal Strength
Signal strength
Rib Cage
Abdomen
3950
3940
3950
3940
3930
3930
3920
3920
3910
3910
3900
3900
3890
3890
3880
3880
Chest Filtered
A
Abdomen Filtered
Time (30-second interval)
Chest Filtered
B
Abdomen Filtered
C
Abdominal Hernia and Diaphragm Force and Velocity
Seated
1. Lung Volume
Increases and the
Diaphragm Shortens:
Force Decreases
FORCE
Standing
2. Increased
Velocity
Reduces
Force
VELOCITY
3. Accessory
Muscle
Recruitment
Increases Force