Pleural pressure increases during inspiration in the zone of apposition of diaphragm to rib cage

The zone of apposition of diaphragm to rib cage provides a theoretical mechanism that may, in part, contribute to rib cage expansion during inspiration. Increases in intra-abdominal pressure (Pab) that are generated by diaphragmatic contraction are indirectly applied to the inner rib cage wall in the zone of apposition. We explored this mechanism, with the expectation that pleural pressure in this zone (Pap) would increase during inspiration and that local transdiaphragmatic pressure in this zone (Pdiap) must be different from conventionally determined transdiaphragmatic pressure (Pdi) during inspiration. Direct measurements of Pap, as well as measurements of pleural pressure (Ppl) cephalad to the zone of apposition, were made during tidal inspiration, during phrenic stimulation, and during inspiratory efforts in anesthetized dogs. Pab and esophageal pressure (Pes) were measured simultaneously. By measuring Ppl's with cannulas placed through ribs, we found that Pap consistently increased during both maneuvers, whereas Ppl and Pes decreased. Whereas changes in Pdi of up to -19 cmH2O were measured, Pdiap never departed from zero by greater than -4.5 cmH2O. We conclude that there can be marked regional differences in Ppl and Pdi between the zone of apposition and regions cephalad to the zone. Our results support the concept of the zone of apposition as an anatomic region where Pab is transmitted to the interior surface of the lower rib cage.     

Mechanical coupling of the rib cage, abdomen, and diaphragm through their area of apposition

Although volumetric displacements of the chest wall are often analyzed in terms of two independent parallel pathways (rib cage and abdomen), Loring and Mead have argued that these pathways are not mechanically independent (J. Appl. Physiol. 53: 756-760, 1982). Because of its apposition with the diaphragm, the rib cage is exposed to two distinct pressure differences, one of which depends on abdominal pressure. Using the analysis of Loring and Mead as a point of departure, we developed a complementary analysis in which mechanical coupling of the rib cage, abdomen, and diaphragm is modeled by a linear translational transformer. This model has the advantage that it possesses a precise electrical analogue. Pressure differences and compartmental displacements are related by the transformation ratio (n), which is the mechanical advantage of abdominal over pleural pressure changes in displacing the rib cage. In the limiting case of very high lung volume, n----0 and the pathways uncouple. In the limit of very small lung volume, n----infinity and the pathways remain coupled; both rib cage and abdomen are driven by abdominal pressure alone, in accord with the Goldman-Mead hypothesis. A good fit was obtained between the model and the previously reported data for the human chest wall from 0.5 to 4 Hz (J. Appl. Physiol. 66:350-359, 1989). The model was then used to estimate rib cage, diaphragm, and abdominal elastance, resistance, and inertance. The abdomen was a high-elastance high-inertance highly damped compartment, and the rib cage a low-elastance low-inertance more lightly damped compartment. Our estimate that n = 1.9 is consistent with the findings of Loring and Mead and suggests substantial pathway coupling.     

Action of the diaphragm on the rib cage inferred from a force-balance analysis

Displacements of the rib cage are determined by the intrinsic passive properties of the rib cage, rib cage musculature, pleural and abdominal pressures, and the diaphragm. The diaphragm's mechanical actions on the rib cage are inferred from a force-balance analysis in which the diaphragm is seen to cause expansion of the rib cage by pulling cephalad at its insertions on the lower ribs (insertional component) and by raising intra-abdominal pressure, which pushes outward on the diaphragm's zone of apposition to the rib cage (appositional component). Goldman and Mead suggested that the diaphragm, acting alone, could drive both the rib cage and abdomen on their passive characteristics. The force-balance analysis shows that the diaphragm's inspiratory action on the rib cage is less than predicted by Goldman and Mead, but that in the special circumstances of their experiment (low lung volumes), the appositional component is large and the rib cage can be driven close to its passive characteristics. The force-balance analysis is consistent with recent observations by other investigations and is incompatible with the model proposed by Macklem and colleagues and with the Goldman-Mead hypothesis. Experiments on three subjects produced data consistent with the force-balance analysis, showing that the inspiratory action of the diaphragm on the rib cage is greatest at low lung volumes.     

Pleural pressure between diaphragm and rib cage during inspiratory muscle activity

We measured the changes in pleural surface pressure (delta Ppl) in the area of apposition of the rib cage to the diaphragm (Aap) in anesthetized dogs during spontaneous breathing, inspiratory efforts after airway occlusion at functional residual capacity, and phrenic stimulation. Intact dogs were in supine or lateral posture; partially eviscerated dogs were in lateral posture. delta Ppl,ap often differed significantly from changes in abdominal pressure (delta Pab); sometimes they differed in sign (except during phrenic stimulation). Changes in transdiaphragmatic pressure in Aap (delta Pdi,ap) could be positive or negative and were less in eviscerated than in intact dogs. delta Pdi,ap could differ in sign among respiratory maneuvers and over different parts of Aap. Hence average delta Pdi,ap should be closer to zero than delta Pdi,ap at a given site. Since delta Ppl,ap = delta Prc,ap, where Prc,ap represents rib cage pressure in Aap, delta Pdi,ap = delta Pab - delta Prc,ap. Hence, considering that delta Pab and delta Prc depend on different factors, delta Pdi,ap may differ from zero. This pressure difference seems related to the interaction between two semisolid structures (contracted diaphragm and rib cage in Aap) constrained to the same shape and position.     

Respiratory effect of the lower rib displacement produced by the diaphragm

The diaphragm acting alone causes a cranial displacement of the lower ribs and a caudal displacement of the upper ribs. The respiratory effect of the lower rib displacement, however, is uncertain. In the present study, two sets of experiments were performed in dogs to assess this effect. In the first, all the inspiratory intercostal muscles were severed, so that the diaphragm was the only muscle active during inspiration, and the normal inspiratory cranial displacement of the lower ribs was suppressed at regular intervals. In the second experiment, the animals were given a muscle relaxant to abolish respiratory muscle activity, and external, cranially oriented forces were applied to the lower rib pairs to simulate the action of the diaphragm on these ribs. The data showed that 1) holding the lower ribs stationary during spontaneous, isolated diaphragm contraction had no effect on the change in lung volume during unimpeded inspiration and no effect on the fall in pleural pressure (Ppl) during occluded breaths; 2) the procedure, however, caused an increase in the caudal displacement of the upper ribs; and 3) pulling the lower rib pairs cranially induced a cranial displacement of the upper ribs and a small fall in Ppl. These observations indicate that the force applied on the lower ribs by the diaphragm during spontaneous contraction, acting through the interdependence of the ribs, is transmitted to the upper ribs and has an inspiratory effect on the lung. However, this effect is very small compared to that of the descent of the dome.     

Cervical magnetic stimulation as a method to discriminate between diaphragm and rib cage muscle fatigue

Inspiratory muscle fatigue can probablydetermine hypercapnic respiratory failure. Diaphragm fatigue isdetected by electrical phrenic stimulation (ELS), but there is nosimple tool to assess rib cage muscle (RCM) fatigue. Cervical magneticstimulation (CMS) costimulates the phrenic nerves and RCM. We reasonedthat changes in transdiaphragmatic pressure twitch (Pdi,tw) with CMSand ELS should be different after selective diaphragm vs. RCM fatigue. Five volunteers performed inspiratory resistive tasks while voluntarily uncoupling diaphragm and RCM. BaselinePdi,tw_ELS andPdi,tw_CMS were 28.57 ± 1.68 and 32.83 ± 2.92 cmH₂O. Afterselective diaphragm loading,Pdi,tw_ELS andPdi,tw_CMS were reduced by 39 and26%, with comparable decreases in gastric pressure twitch (Pga,tw).Esophageal pressure twitch (Pes,tw) was better preserved with CMS.Therefore Pes,tw/Pga,tw was lower with ELS than CMS (1.24 ± 0.16 vs. 1.73 ± 0.11, P = 0.05). After selectiveRCM loading, there was no diaphragm fatigue, butPes,tw_CMS was significantlyreduced (30%). These findings support the role of rib cagestiffening by CMS-related RCM contraction in the ELS-CMSdifferences and suggest that CMS can be used to assess RCM fatigue.

     

Effect of rib cage and abdominal restriction on total respiratory resistance and reactance

In 14 healthy male subjects we studied the effects of rib cage and abdominal strapping on lung volumes, airway resistance (Raw), and total respiratory resistance (Rrs) and reactance (Xrs). Rib cage, as well as abdominal, strapping caused a significant decrease in vital capacity (respectively, -36 and -34%), total lung capacity (TLC) (-31 and -27%), functional residual capacity (FRC) (-28 and -28%), and expiratory reserve volume (-40 and -48%) and an increase in specific airway conductance (+24 and +30%) and in maximal expiratory flow at 50% of control TLC (+47 and +42%). The decrease of residual volume (RV) was significant (-12%) with rib cage strapping only. Abdominal strapping resulted in a minor overall increase in Rrs, whereas rib cage strapping produced a more marked increase at low frequencies; thus a frequency dependence of Rrs was induced. A similar pattern, but with lower absolute values, of Rrs was obtained by thoracic strapping when the subject was breathing at control FRC. Xrs was decreased, especially at low frequencies, with abdominal strapping and even more with thoracic strapping; thus the resonant frequency of the respiratory system was shifted toward higher frequencies. Partitioning Rrs and Xrs into resistance and reactance of lungs and chest wall demonstrated that the different effects of chest wall and abdominal strapping on Rrs and Xrs reflect changes mainly of chest wall mechanics.     

Zone of apposition in the passive diaphragm of the dog

Boriek, Aladin M., Joseph R. Rodarte, and Susan S. Margulies. Zone of apposition in the passive diaphragm of thedog. J. Appl. Physiol. 81(5): 1929-1940, 1996.Wedetermined the regional area of the diaphragmatic zone of apposition(ZAP) as well as the regional craniocaudal extent of the ZAP(ZAP_ht) of the passive diaphragm in six paralyzedanesthetized beagle dogs (8-12 kg) at residual lung volume (RV),functional residual capacity (FRC), FRC + 0.25 and FRC + 0.5 inspiratory capacity, and total lung capacity (TLC) in prone and supinepostures. To identify the caudal boundary of the ZAP, 17 lead markers(1 mm) were sutured to the abdominal side of the costal and cruraldiaphragms around the diaphragm insertion on the chest wall. Two weekslater, the dogs' caudal thoraces were scanned by the use of thedynamic spatial reconstructor (DSR), a prototype fast volumetric X-raycomputer tomographic scanner, developed at the Mayo Clinic. Thethree-dimensional spatial coordinates of the markers were identified(±1.4 mm), and the cranial boundary of the ZAP was determined from30-40 1.4-mm-thick sagittal and coronal slices in each DSR image.We interpolated the DSR data to find the position of the cranial andcaudal boundaries of the ZAP every 5° around the thorax and computedthe distribution of regional variation of area of the ZAP andZAP_ht as well as the total area of ZAP. TheZAP_ht and area of ZAP increased as lung volume decreasedand were largest near the lateral extremes of the rib cage. We measuredthe surface area of the rib cage cephaled to the ZAP(A_L) in both postures in another six beagle dogs(12-16 kg) of similar stature, scanned previously in the DSR. Weestimated the entire rib cage surface area(A_rc = A_ZAP +A_L). The A_ZAP as a percentageof A_rc increased more than threefold as lung volumedecreased from TLC to RV, from ~9 to 29% of A_rc.

     

Hox patterning of the vertebrate rib cage

Unlike the rest of the axial skeleton, which develops solely from somitic mesoderm, patterning of the rib cage is complicated by its derivation from two distinct tissues. The thoracic skeleton is derived from both somitic mesoderm, which forms the vertebral bodies and ribs, and from lateral plate mesoderm, which forms the sternum. By generating mouse mutants in Hox5, Hox6 and Hox9 paralogous group genes, along with a dissection of the Hox10 and Hox11 group mutants, several important conclusions regarding the nature of the ;Hox code' in rib cage and axial skeleton development are revealed. First, axial patterning is consistently coded by the unique and redundant functions of Hox paralogous groups throughout the axial skeleton. Loss of paralogous function leads to anterior homeotic transformations of colinear regions throughout the somite-derived axial skeleton. In the thoracic region, Hox genes pattern the lateral plate-derived sternum in a non-colinear manner, independent from the patterning of the somite-derived vertebrae and vertebral ribs. Finally, between adjacent sets of paralogous mutants, the regions of vertebral phenotypes overlap considerably; however, each paralogous group imparts unique morphologies within these regions. In all cases examined, the next-most posterior Hox paralogous group does not prevent the function of the more-anterior Hox group in axial patterning. Thus, the ;Hox code' in somitic mesoderm is the result of the distinct, graded effects of two or more Hox paralogous groups functioning in any anteroposterior location.     

Patterns of shortening and thickening of the human diaphragm

Wait, J. L., and R. L. Johnson. Patterns of shorteningand thickening of the human diaphragm. J. Appl.Physiol. 83(4): 1123-1132, 1997.To study how the human diaphragm changesconfiguration during inspiration, we simultaneously measured diaphragmthickening using ultrasound and inspired volumes using apneumotachograph. Diaphragm length was assessed by chest radiography.We found that thickening and shortening were greatest during a breathtaken primarily with the abdomen. However, the degree of thickening wasgreater than expected for fiber shortening, assuming parallel musclefibers and no shear. So, to clarify this unexpected finding, weconsidered geometric models of the diaphragm. How a muscle thickens asits fibers shorten is critically dependent on geometry. Thus, if a flatrectangular sheet of muscle shortens along one dimension, surfacearea-to-length ratio along this dimension should remain constant, andthickness would be inversely proportional to length during shortening.The simplest model of the diaphragm, however, is a cylindrical sheet ofmuscle in the zone of apposition capped by a dome; the ratio of surfacearea to radial fiber length in the dome is substantially less than theratio of area to length of the cylindrical zone of apposition; hence,as the zone of apposition shortens while the dome radius remainsconstant, the ratio of total surface area to combined length (i.e.,dome + zone of apposition) must decrease and thickening of the musclecorrespondingly must increase more than expected for a simplerectangular strip. A similar relationship can be derived betweenthickening and length in a muscle sheet with a wedge-shaped insertioninto a thin flat tendon. Comparison of calculations with these types ofmodels to data from human subjects indicates that the unexpectedthickening in the zone of apposition is explained by the peculiargeometry of the diaphragm. The greater thickening of the diaphragm inthe zone of apposition suggests that more of the muscle mass and more sarcomeres are retained in the zone of apposition as the dome descends.Physiologically, this greater thickening may have importance byreducing wall stress in the zone of apposition and reducing the work orenergy requirements per sarcomere.