Aging and theRespiratory System

Lorenzo Bonomo, MDa,*, Anna Rita Larici, MDa, FabioMaggi, MDa,Francesco Schiavon, MDb, Riccardo Berletti, MDb

KEYWORDS� Elderly � Respiratory system � Radiologic modifications

Radiologic tests are performed on elderly patients(conventionally defined as individuals 65 yearsof age and older) with increasing frequencybecause of the progressive increase in the averageage, owing to better life conditions and toprogress in medical, surgical, and anaesthesio-logic knowledge.1

In the elderly, it is often difficult to establishwhat normality, or rather, what ‘‘compatibility,’’is, because of the numerous anatomic and physi-ologic modifications that occur during the agingprocess. As a result, the major problem in laterlife is to recognize the point to which aging isnormal and the point at which the disease begins.2

The overall anatomic/radiologic modifications ofthe thorax that occur with advanced age aresummarized in Box 1. The authors then discussthem in greater detail.

THORACIC FRAME

The thoracic frame may be subdivided into (1) thethoracic wall and (2) the diaphragm.

Thoracic wall

Reduction in wall thickness is constant and is wellshown by computed tomography (CT), particularlywhen compared with younger individuals (Fig. 1).This reduction is one of the principal causes ofhyperlucency in the elderly chest.3

Islands of compact matter and bony, costalreparatory calluses are common, as is calcificationof the costal cartilage. In general, the cartilagecalcifies according to the standard defined, that

a Department of Bioimaging and Radiological SciencesAgostino Gemelli, L.go F. Vito 8, 00168 Rome, Italyb Department of Imaging Diagnostics and Radiologica32100 Belluno, Italy* Corresponding author.E-mail address: lbonomo@rm.unicatt.it (L. Bonomo).

Radiol Clin N Am 46 (2008) 685–702doi:10.1016/j.rcl.2008.04.0120033-8389/08/$ – see front matter ª 2008 Elsevier Inc. All

is, in the periphery in men and in the center inwomen, but sometimes, although not often, withnodular appearance.2

These alterations give rise to differential diag-nosis problems with respect to nodular pulmo-nary lesions. Three factors need to be takeninto consideration: first, in the elderly, radio-scopy is not always reliable because of limitedpatient cooperation and possible reduction ofrespiratory excursions; second, lung cancer ismost frequent between the ages of 60 and 70,often in the form of peripheral nodes (adenocar-cinoma); third, postthoracotomy mortality in theelderly today is close to that of younger adultsand the diagnostic commitment must thereforebe the same.4

The principal modifications of the spinal columnare osteoporosis, consistent with age if notassociated with subjective disturbances (‘‘elderly’’osteoporosis), and osteophytosis, generally morepronounced on the right side of the vertebralcolumn because of the protection of the aorta onthe left side. This occurrence is also a source ofproblems of differential diagnosis with respect toposterior pulmonary nodules, along with costo/transversal arthrosis (it may be useful for diagnos-tic purposes to consider the side on which thedoubtful image appears: if on the right side, de-generative alteration is more probable; if on theleft side, the hypothesis of pulmonary lesion maybe more consistent) (Fig. 2). Accentuation of thedorsal kyphosis, associated with the greater con-vexity of the sternum, contributes to the ‘‘barrel’’thorax configuration (Fig. 3).

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Box1Anatomic/radiologic modifications in the chest inthe elderly

Frame

Soft tissues

Hypotonia and muscular hypertrophy

Distribution

Reduction of fat

Ribs

Decalcification

Depletion

Cartilaginous calcification

Vertebrae

Decalcification

Kyphoscoliosis

Arthrosis

Deformation

Diaphragm

Widening of the hiatuses

Parietal anterior/posterior modifications

‘‘Bell’’ chest

Vertebral interior/posterior modifications

‘‘Barrel’’ chest

Mediastinum

Heart

Coronary arteriosclerosis

Increase in adipose tissue

Muscular hypertrophism

Thickening of the endocardium

Rheumatic-like valvular margins

Aorta

Arteriosclerosis

Ectasia

Lengthening

Trachea

Parietal malacia

Pulmonary arteries

Arteriosclerosis

Lung

Macroscopically

Increase in support tissue

Enlargement of the distal airspaces

Reduction of capillary bed

Possible terminal bronchiolitis

Microscopically

Increase in collagen

Modification of elastin

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All of these parietal modifications lead to hard-ening of the thoracic cage, with unfavorablerebound on respiratory function.5–7

Diaphragm

Although nearly always in a normal position, thediaphragm often shows protuberances and isstippled because of muscular hypertrophy anddyskinesia, particularly on the right, probablycaused by the increased effort by the hemidiaph-ragm in maintaining the anatomic relationshipbetween the lung and the liver. The anatomic hia-tuses are generally wider, and hernias are morefrequently found and may resemble mediastinaland paramediastinal masses.6

The presumed ‘‘bulges’’ of the diaphragm mayalso constitute diagnostic traps, making differen-tial diagnosis necessary with thoracic diseasesthat lower the diaphragm and with abdominalmasses that raise it (Fig. 4). It is therefore impor-tant, when the position of the diaphragm is differ-ent from the norm, to determine its positionprecisely. Echography may be of use in this caseand in suspected infrapulmonary effusion, fre-quent in the hemodynamically decompensatedelderly (Fig. 5).

The lowering of the diaphragm may be due, inaddition to pleural effusion, to cardiomegaly,which increases the weight of the heart on thediaphragm (see later discussion).

MEDIASTINUM

The modifications of most interest concern theheart, the aorta, and the trachea.

Heart

The anatomic/pathologic aspects of the ‘‘elderlyheart’’ essentially refer to what is known as‘‘primary’’ aging, that is, to a limited and fortunatepercentage of healthy elderly (approximately10%). These individuals are best suited for assess-ment of modifications caused by age only,whereas ‘‘secondary’’ aging, that is, the muchmore frequent situation influenced by basicpathologic conditions (arterial hypertension, ath-erosclerotic, pulmonary emphysema and chronicbronchitis, diabetes mellitus, renal insufficiency,and so forth) or by an unhealthy lifestyle (reducedphysical activity, improper diet, abuse of alcoholand tobacco) is obviously excluded, being influ-enced by too many individual variables.8,9

The principal involutions that characterize the‘‘elderly heart’’ are an increase in the cardiacmass and the thickness of the myocardium, ofthe left ventricle in particular, due to hypertrophy

Fig.1. With advanced age comes progressive atrophy of the muscles of the thoracic wall, responsible for a signif-icant increase in thoracic radiotransparency when radiographic tests are performed, because of lower reductionof the radiogenic beam. It is a question of an apparent increase in pulmonary transparency, which can beattributed to lower contribution to the parietal opacity rather than an actual alteration of the pulmonary paren-chyma (emphysema). (A) Axial CT scan of the chest of a young individual with good tropism of the parietal mus-culature. (B) Axial CT scan of the chest of an elderly patient who has evident muscular atrophy, particularly of thepectoral muscles and those of the posterior wall.

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of the residual myocytes and to an increase in thematrix of connective tissue; thickening of the val-vular margins (often mitral and aortic) due to thedeposit of fats, collagen, and calcium salts, withinitial wearing out of the valvular annulus which,at the mitral level, causes a slight insufficiency in90% of those over the age of 80; coronary sclero-sis, with possible alterations of the cardiac perfu-sion.8–14

Fig. 2. Arthrosis of the costo-vertebral joint. The chest rada doubtful pulmonary nodular lesion projecting against thsequently performed (B) reveals the degenerative nature

In any case, apart from the involutions describedin ‘‘primary’’ aging, every significant morphodi-mensional variation of the heart must be consid-ered as a possible sign of alteration of theintrinsic or extrinsic hemodynamics.10

In most cases, the signs of right cardiac over-load are due to an increase in the resistance ofsmall pulmonary vessels, as in the case of ob-structive or restrictive diseases and mitral defects,

iograph in lateral projection (A) shows the image ofe spinal column (circle). The CT scan of the chest sub-

of the radiographic finding (circle).

Fig. 3. Aging causes a reduction in the calcium contentof the bones and involutive alterations that may re-sult in fractures and deformations of thoracic cagestructures. Radiograph of the chest in lateral projec-tion: ‘‘barrel’’ chest, due to accentuation of the dorsalkyphosis and convexity of the sternum.

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whereas the signs of left overload (ie, left ventriclehypertrophy) may partially be due to modificationsof the ‘‘elderly heart.’’11

Calcification of the thoracic aorta, of the cardiacvalves (margins and annulus), and of the coronaryarteries (often of the descending left anteriorbranch) must be checked for, because they indi-cate, in the elderly, those individuals subject toa risk for cardiovascular pathology (Fig. 6).2,13

Thus, in addition to the coronary circulation, the‘‘elderly heart’’ has two attack points: themyocardial structures and the cardiac valves.

Fig. 4. In the elderly, it is not always easy to identify the examodifications caused by aging and the presence of masdiaphragm. An example is given here: in the frontal rawas first suggested, but the evidence of the homolateral insumed hemidiaphragm, resulted in the correct diagnosis, lanary mass.

Both can be assessed with imaging, producingtwo histopathologic and clinical aspects of partic-ular importance: increase in the weight of the heartand double genesis of cardiac, systolic, anddiastolic decompensation,14 which are discussedin more detail below.

Aorta

Essentially, the aorta’s anatomic/pathologic mod-ifications can be added to those of the heart, andresult in lengthening and dilation, factors princi-pally responsible for enlargement of mediastinalcontours in chest radiograph frontal projections.15

In general, the lengthening is greatest in the cra-nial direction and the calibre of the aortic arch,measurable, for example, on the transparency ofthe tracheal air column, may reach up to 4 cm ormore (Fig. 7). But differential diagnosis must al-ways be considered with intrinsic alterations,such as aneurysm, or with extrinsic alterations,such as masses of the contiguous mediastinalstructures.8

The almost constant atheromatic calcification,often of the arch and of the descending section,do not always relate to the gravity of the clinical sit-uation, and may be associated with variousconditions (such as chronic renal insufficiencyand so forth).9,15

Trachea

The trachea is an important anatomic reference inassessing the condition of the superior mediasti-num. It is visibly deviated to the right from the aor-tic arch in 30% of cases, sometimes resemblingmediastinal involvement.6 In this case, locatingthe right paratracheal line and the normality of

ct position of the hemidiaphragms because of intrinsicses or liquids that can collect above and below thediograph (A), hyperelevation of the hemidiaphragmferior cardiac contour, caudal with respect to the pre-ter confirmed by CT (B), which showed a basal pulmo-

Fig. 5. Infrapulmonary pleural effusion. (A) Standard chest radiograph: signs of initial CD with infrapulmonaryeffusion, most visible on the left, due to an increase in the normal distance between the lung and the colicflexure, with involvement of the costal-phrenic sinus. (B) Echographic scans of the left hypochondrium, whichconfirmed the presence of infrapulmonary effusion.

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the homolateral mediastinal space, correspondingto the innominate/caval axis, assists in correctassessment (Fig. 8). The frequent presence ofcatheters or pacemaker electrodes in the superiorvena cava of elderly patients helps in theassessment of the vascular nature of the enlargedmediastinum.4,6

Fig. 6. In the elderly, the coronary arteries become tor-tuous and often present deposits of calcium salts andatherosclerotic plaque. The aorta undergoes similaralterations; the cardiac valvular apparatus also showscalcium deposits (particularly at the level of the aorticvalve and the mitral annulus). Chest radiograph in lat-eral projection: vascular and valvular calcifications.

The trachea may present a ‘‘saber-like’’ appear-ance, often in a bronchitic/emphysematous con-text, because of parietal malacia that increasesthe tracheal antero-posterior diameter and tendsto cause the collapse of the lateral walls(Fig. 9).7,16

LUNG

Parenchymal modifications are caused by re-duced blood flow from the systemic circulationthrough the bronchial arteries and by the reduced

Fig. 7. Modifications of the thoracic aorta associatedwith aging. The chest radiograph in lateral projectionshows an increase in the vessel’s calibre and length.

Fig. 8. In the elderly, tracheal deviations arefrequently found: study of the relationships with con-tiguous anatomic structures and analysis of themediastinal lines and spaces are of assistance in diag-nosis. The chest radiograph taken of a supine patientshows a deviation to the right of the trachea due toectasia of the aortic arch.

Bonomo et al690

function of the cellular membranes, and result inquantitative/qualitative modifications to collagenand variations in the relationship between elastictissue and support tissue, with progressive reduc-tion of lung elasticity.6,7

The first physiopathologic consequence is prox-imal shifting of the closing point of the distalairways, with a progressive increase in residual

Fig. 9. ‘‘Saber-sheath’’ trachea. The standard chestradiograph shows pulmonary emphysema, withreduction of the tracheal calibre on the frontal plane.

volume. This mechanism is analogous to that ofpulmonary emphysema, with two major differ-ences: no signs of inflammation and no increasein total pulmonary capacity.17,18

At the same time, the ventilation/perfusionrelationship is modified because of a reduction inthe number of alveoli with optimal gas exchange,which has two physiopathologic consequences:an increase in the physiologic dead space andthe ‘‘shunt effect,’’ with a reduction of arterialoxygenation.7,18

From the radiologic point of view, these modifi-cations translate into what is known as the ‘‘dirtychest,’’ caused by the increase of supportingconnective tissue (ie, of the interstitium), whichbecomes a normal component of the chest radio-graph, adding to and becoming superimposed onvascular trauma (Fig. 10), and by the increase inthe background transparency of the chest, causedby an increase in the pulmonary air content,a reduction in vascularization, and reduced thick-ness of the thoracic wall (Fig. 11).6,7

In addition, modest pulmonary hypertension (aclinical expression of vascular involution) maymake occupation of the ‘‘reserve’’ vascular areacommon in the elderly, inhibiting use of redistribu-tion of the pulmonary flow as a first radiologic signof cardiac decompensation (CD). In such cases,left CD may be assessed only by later signs,such as the shaded appearance of hilar structuresand vascular contours, which are an indication ofinterstitial edema.19–21

Although in younger adults the calibre of theprincipal pulmonary arteries is related to arterial

Fig. 10. Elderly patient who has severe functionalobstruction detected with respiratory functional testsand evidenced by longstanding productive cough.The radiographic examination of the chest showsa ‘‘dirty lung,’’ with significant accentuation of bron-chovascular findings (increased markings).

Fig. 11. Elderly individual with medium-degree ob-struction detected with respiratory functional tests.Radiographic evidence of emphysema with pulmonaryhyperinsufflation and reduction of the vasal picture(arterial deficiency) due to hypertension of the lessercirculation, documented by dilation of the descendingbranch of the right pulmonary artery (arrow).

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pulmonary pressure, in the elderly this may nolonger be the case, because a certain degree ofpulmonary atherosclerosis and sometimes em-physema (confirmed by anatomic/pathologicfindings), is always present. For this reason, ath-erosclerosis and pulmonary hypertension forma closed circle, each contributing to the other, asis found paraphysiologically in the elderly.20,21

The role of multiple and repeated episodes ofpulmonary embolism, fibrosis, and mitral stenosismust also be taken into consideration in the gene-sis of pulmonary hypertension in the elderly,among whom all of the foregoing are frequentpathologic and clinically silent conditions.18,19

Enlargement of the distal airspaces (see laterdiscussion) may provoke compression and reduc-tion of the capillary arterial bed, which mightexplain any peripheral hypoperfusion.17,20 Thisfinding is common among bedridden, inactive el-derly patients, probably also because of a de-crease in the cardiac output. In fact, because thechest radiographs of physically active and healthyelderly individuals show no signs of hypoperfu-sion, it may be deduced that the more inactivethe elderly individual is, the lower effectiveperfusion present.21

Involution of respiratory function begins as earlyas 30 years of age, as shown by spirometric tests.The curve of forced expiratory volume in 1 secondfalls slowly and inexorably until reaching, atadvanced age, values at the limits of survival.18

In addition to involution of the parietal thoraciccomponent with aging is a significant restructuring

of the pulmonary architecture, due particularly toan increase in the collagen and elastin of thebronchial walls and interstitium, expressed radio-logically with the picture of the ‘‘dirty chest,’’ men-tioned previously.

These modifications to the pulmonary architec-ture result in enlargement of the distal airspacesand a reduction of the extension of the intra-alveolar septa.16,22

The internal surface of the lung thus diminishesfrom an average of 70 m2 at 30 years of age to60 m2 at 70 years. In other words, in the thirddecade of life, in step with the decreased ex-piratory flow comes a loss of pulmonary alveolarsurface, amounting to 4% per decade, whichis known as reduction of the ventilatorysurface.23,24

The ensuing radiologic aspects (also taking intoconsideration the increase in residual volume) arethe following: bronchial and bronchiolar expiratorycollapse, often posterior/basal; small dependentgravitational thickening; and dependent subpleu-ral linear atelectasis.17

In particular, CT regularly shows a slight halo ofhyperdensity in the dependent subpleural areas,which disappears when the position of the patientis changed (Fig. 12). This picture is essentiallya representation of the radiologic aspects previ-ously listed.17,25

The slight hyperdistension of the alveoli, withdilation of the respiratory bronchioles and con-comitant reduction of the alveolar capillaries,could result in a picture of centrilobular emphy-sema. In reality, the signs and symptoms of trueemphysema (dyspnea, cough, and so forth) areabsent in the ‘‘elderly lung.’’ In addition, even ifthe elderly person becomes polypneic at restand under stress, and the current volume dimin-ishes (that is, the quantity of air ventilated witheach respiratory act), the inflammatory aspectsand increase in the total pulmonary capacity, typ-ical of pulmonary emphysema, are absent. Forthese reasons, ‘‘elderly emphysema’’ does notexist as a distinct clinical/radiologic entity.23

It is, however, true that the progressive ‘‘reduc-tion’’ of the parietal/alveolar tissue may result inalveolar ruptures and hence in the formation of 2to 3 cm blisters, located particularly in the upperand anterior part of the lung. Furthermore, the ter-minal bronchioles often show an acute or chronicinflammatory process, particularly in the elderlywith a history of smoking. But, in general, emphy-sema, when radiographically demonstrable, is anadvanced process from anatomic and physiopath-ologic points of view, insofar as its early phase isconfused, or rather, is consistent, with the normalelderly chest.23,24

Fig.12. Dependent parenchymal hyperdensity is a frequent CT finding, particularly in the elderly. The cause seemsto be a diminishing of the closing pressure of the most distal airways, which facilitates bronchial collapse, asso-ciated with lines of parenchymal dysventilation with analogous physiopathologic significance. This aspect isreversible by varying the body position. The CT scan performed in a supine position (left) shows ‘‘ground glass’’dependent hyperdensity of the pulmonary base, which disappears when the patient is placed in a prone position(right) because of a variation in blood pressure conditions.

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PRINCIPAL PHYSIOPATHOLOGICMODELS

Once the principal involutions of thoracic struc-tures have been described, one can observe twophysiopathologic models most common in theelderly: the ‘‘cardiac lung’’ (CL) and the ‘‘pulmo-nary heart’’ (PH), the clinical expressions of whichare, respectively, cardiogenic pulmonary edema(ie, CD) and chronic obstructive pulmonary dis-ease (COPD).

‘‘Cardiac Lung’’

The numerous epidemiologic studies now avail-able agree on the fact that CD is the cause of deathin approximately 80% of subjects over the age of80 and is the most frequent pulmonary and,more generally, internal medical reason for hospi-talization.26 The symptom at the basis of all thepictures attributable to CD is dyspnea and the cor-responding clinical picture is that of pulmonaryedema.27–32

The physiopathologic model at the basis of CD,as explained by the clinical presentation, is theCL.30

The definition of the CL derives from a simpleconsideration: the two pumps in the chest, thecardiac and the pulmonary, are vital and must bein perfect balance for optimal functioning. Thefunctional insufficiency of one inevitably hasconsequences for the other.28 This considerationconcerns the impact of primitive pulmonary pa-thology on the heart, known as the PH, which the

authors discuss below, and the impact of primitivecardiac diseases on the lung that is, the CL.29–31

In the CL, the situation reproduced in Fig. 13 iscreated. The enlarged heart occupies more spacein the thoracic cavity (which is nonexpandable)than it should, to the detriment of the lungs, whichreduce their respiratory excursions. Imbalance isthus created between the pumps, with the cardiacpump dominating the pulmonary pump.28

The authors discussed the ‘‘elderly heart’’ ear-lier. Two factors result: an increase in the weightof the heart and the double genesis of systolicand diastolic CD.

An increase in the weight of the heart is easilyvisible in a patient equipped with a pacemakerand in whom the position of the stimulating probein the right ventricle shows a lowering of the dia-phragm, due to the weight of the heart (Fig. 14).This aspect is a further cause of dyspnea (andhence of respiratory insufficiency) in patients whohave CD, because it has an unfavorable effect onthe work of the diaphragm, which is the principalinspiratory muscle. Thus, correction of the cardi-opathy is positively reflected in respiratoryperformance.30

The distinction between systolic and diastolicCD represents a significant challenge for the radi-ologist because the clinical contexts are differentand important: ischemic cardiopathy for the for-mer, systemic arterial hypertension for the latter.In particular, it has been shown that, in those olderthan 65, 40% of CD has diastolic causes, which

Fig.13. The principal physiopathologic characteristic of the CL is the imbalance created between the cardiac pumpand the respiratory pump because of enlargement of the heart, which occupies a large part of the chest to thedetriment of the lungs, with reduction of respiratory excursions and alteration of the ventilation/perfusiondynamics. Standard radiograph (A) and CT (B) of the chest: enlargement of the heart, particularly of the leftcavity, with signs of redistribution of the pulmonary circulation, due to recruitment of the ‘‘reserve’’ area.

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constitute a significant practical problem, becausethe therapeutic approach is different.33–38

The physiopathology of systolic CD involves thedilation of the left ventricle, without alteration inwall thickness, and a reduction of the ejection frac-tion. For diastolic CD, parietal thickening of the leftventricle occurs without dilation, with a negativeeffect on the rates of diastolic refilling and normalstate of the ejection fraction.36–38

Chest radiograph is fundamental for distinguish-ing between the two types of failure and is closelyrelated to the physiopathology. In both forms, the

Fig.14. Chest radiograph in lateral projection. Increasein the weight of the heart in a patient fitted witha pacemaker is shown by the extreme distal positionof the stimulating electrode (circle), providing evi-dence of the lowering of the left hemidiaphragm.

appearance of pulmonary circulation, that typicalof CD and described later, is similar, whereasthat of the heart is different: enlarged in systolicCD, within the limits in diastolic CD (Fig. 15).33,39

The authors now describe the principal, associ-ated, and subsequent radiologic pictures of theCL, relating them to the physiopathologic events,while bearing in mind that such a representationis of explanatory use only (Fig. 16).28,31 The entireprocess is summarized in Table 1.

Picture I: reduction of the cardiac range, withvenous stasis and increase in the intravascularpulmonary liquidThe increase in pulmonary haematic volume (ie,the venous stasis) is first of all expressed by redis-tribution of the vessels in the caudal/cranial direc-tion, as an expression of recruitment of the‘‘reserve’’ area, and hence by an increase in theircalibre. They thus maintain clear contours. Theheart may, although not necessarily, have signsof moderate enlargement of the left atrium. Thelungs and heart increase in weight because ofthe venous stasis, resulting in insufficient pumpfunction, which provokes further lowering of theleft hemidiaphragm; in normal condition the righthemidiaphragm is higher than the left not becauseof the pressure from the liver but because of theweight of the heart (in particular ventricles) on theleft hemidiaphragm.

Picture II: increase in extravascularpulmonary liquidSigns of liquid effusion, that is, of interstitialedema, appear in the interstitium. They includeshading of the vascular picture and of the hilarstructures, the Kerley lines, particularly type B,

Fig.15. Systolic versus diastolic CD. (A) Standard chest radiograph: systolic CD is characterized by signs of pulmo-nary stasis and by enlargement of the heart, particularly of the left sections, due to deficit in the systolic functionof the left ventricle. (B) Standard chest radiograph: in diastolic CD, the signs of pulmonary circulation overloadare associated with concentric hypertrophy of the left ventricle, without significant increase in its size. Thiscondition is, in fact, characterized by a reduction of the ventricular telediastolic volume without deficit of systolicfunction (election fraction >45%). Other causes of failure, such as anemia, thyrotoxicosis, valvular diseases, and soforth, are, in any case, excluded.

Fig.16. Phases of cardiogenic failure. Chest radiographs of the same patient, from simple venous overload to ev-ident pulmonary edema. (A) The CL in relative hemodynamic compensation. (B) Signs of interstitial edema withpleural effusion and enlargement of the cardiac image. (C) Alveolar edema with extended parenchymal opacities,increase in pleural effusion, and further enlargement of the heart.

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Table1Main radiologic, clinical, and instrumental characteristics of the ‘‘cardiac lung’’

Clinical/InstrumentalCharacteristics Radiologic Characteristics

Stage I Y Clinical range[ Pulmonary hematic volume

Caudal/cranial redistribution of the pulmonarypicture (‘‘reversed’’ distribution)1/1 relationshipbetween superior/inferior vessel calibres(‘‘balanced distribution’’)

Stage II Dyspnea [Extravascular liquid[HGA 1 � (under stress)

Interstitial edema (Kerley lines, shaded hila,pleural effusion)

Heart 1Pulmonary volume Y

Stage III As in stage II As in stage II, with gravitational distribution,often bilateral pleural effusion

Stage IV Dyspnea [[Obligatory seated position

Heart 11Lowering of diaphragm[[

Stage V Dyspnea [[[HGA � �

Lowering of diaphragm[[[Thickening of thoracic wall [[

Stage VI Dyspnea [[[[HGA � � � �

Gravitational, confluent and shaded parenchymalopacities. Bilateral pleural effusion

Heart 1111Lowering of the diaphragm[[[

Abbreviations: 0, normal; 1, enlarged; �, reduced; [, increased; Y, reduced; HGA, hemogas analysis.

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moderate subpleural parenchymal thickening, en-largement of the diameters of the heart with moreevident enlargement of the left cavities, and possi-ble limited pleural effusion. A reduction in respira-tory volume begins, with minor expansion of thethorax as detected by radiograph, plus reductionof respiratory excursions.

Picture III: pleural effusionWhen present (most typically bilaterally), the signsof gravitational edema will already have appeared.Pleural effusion is therefore part of a picture ofmedium-advanced interstitial edema.

Picture IV: evident cardiomegalyThe signs of cardiomegaly and the lowering of thediaphragm predominate, both clearly seen bychest radiograph. The supine hypoxia, typical ofthis phase, is well explained by CT (see laterdiscussion).

Picture V: involvement of the respiratorymuscles and the soft tissuesThe authors have already referred to the loweringof the diaphragm. Imbibition on the wall (typicalof pulmonary edema due to hyperhydration aswell as nephrogenic edema) is, however, of

significance in cardiogenic edema on functionallevel, because respiratory muscles become moreviscous and less efficient, making an increase inthe force they use to move the thoracic cage nec-essary. It is therefore necessary that radiographexamination of the chest also allow assessmentof wall thickness.

Picture VI: appearance of alveolar edemaThis picture is well known, referred to only in theinterests of completeness.

To better understand the mechanisms that gov-ern the process described earlier, a few referencesto functional anatomy are necessary concerningthe diaphragm, pulmonary arteries, alveolar com-partment, lymphatics, and interstitium.20,21

Regarding the diaphragm (the principal inspira-tory muscle), the normal anatomic position andits maintenance are important.

Regarding the pulmonary arteries, the smoothparietal musculature is considerably less repre-sented at all ages, with respect to the systemiccirculation, which in physiologic terms, meansthat the vessels are more distensive and thereforemore prone to increasing rather than reducing theircapacity.

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Regarding the alveoli, the connective tissuebetween type I alveolocytes (ie, the cells thatcover almost the entire alveolar surface) is closedand impermeable, as opposed to that betweenthe endothelial cells of the capillaries, which eas-ily allow the passage of liquid. The surfactant (aphospholipoprotein secreted by type II alveolo-cytes) covers the alveolar wall with water-repel-lent action, enabling ventilation and inhibitingatelectasis.

The alveolar septa (represented by the intersti-tial tissue between the epithelium and endothe-lium) are formed by two functionally distinctareas, one of which is thin, to allow gas exchange,and the other thick, for liquid exchange.

The capillary lymphatics are found at the levelof the alveolar ducts and the respiratory bronchi-oles. The interstitial liquid runs from the alveolarwalls to the capillary lymphatics, driven by the‘‘pump’’ action of the ventilation, which is more ef-ficient in the pulmonary mantle, as shown by the‘‘butterfly wing’’ distribution often observed in car-diogenic alveolar edema (Fig. 17). The lymphmoves from the capillaries through the lymphaticducts with the help of valves at a distance of 1 to2 mm.

The interstitium may be subdivided into twocomponents: a peripheral, parietal, and subpleuralcomponent, thin and radiologically invisible; andanother component found around the bronchiand the vessels (peribronchovascular cuffing), vis-ible with chest radiograph as a small opaque circleof the bronchial walls taken tangentially. Both are

Fig. 17. CD with evident pulmonary edema. The chestradiograph of the supine patient shows characteristic‘‘butterfly wing’’ edema caused by more effective lym-phatic draining of the pulmonary mantle.

connected to a thick reticule made up of the con-nective tissue of the alveolar septa.

The extravascular liquid is first collected in thelarge interstitium because of the more efficient pe-ripheral ventilation and the greater compliance ofthe large interstitium, and, only if insufficient, inthe alveolar septa. In fact, the interstitium is thenatural site for liquid exchange and, when neces-sary, the peribronchovascular connective tissueup to the thickest part of the alveolar septabecomes a large reserve of ‘‘extravascular water,’’which inhibits alveolar flooding, preserving the gasexchanges.29

The lymphatic vessels have an aspiration pres-sure of 20 to 30 cm of H2O on the fluids andsolutes in the interstitium, guaranteed by theexcursions transmitted to them by the transpulmo-nary respiratory pressure. Although able to in-crease the level of drainage considerably, thecapacity of the lymphatic vessels is limited to thelevel of which the liquid passes at the extravascu-lar site, even in consideration of their significantlydisproportionate development with respect to thecapillary network.29

A note on the circulation of the visceral pleura:disagreement exists as to its origin, derivingwholly or partially from the pulmonary arteries ac-cording to some investigators, or from the bron-chial arteries according to others. In any case,its venous draining occurs through the pulmonaryveins.40

The argument presented up to this point regard-ing functional anatomy raises several interestingradiologic observations.41–43

The first sign of venous stasis (phase I), is the‘‘reversed’’ distribution of the flow (ie, with recruit-ment of the reserve vascular area of the superiorlobes) and with ‘‘balanced’’ distribution (ie, withan increase in the calibre of the vessels recruited)(see Fig. 13).

A reduction in the pulmonary compliance (ie, in-creased rigidity of the lung due to an increase inthe interstitial fluid [phase II]) and a rapidly worsen-ing restrictive syndrome result in decreased lungexpansion in the chest radiograph taken in inspira-tory apnea and in a reduction of respiratory excur-sions, if the radiograph is also taken in expiratoryapnea.

The work of the lymphatics at ‘‘low rate’’ todispose of the extravascular liquid is also per-formed when the clinical picture is regressed andthe hemodynamic picture is in the process ofrebalancing, thus explaining the dissociation be-tween clinical and radiologic resolution. In otherwords, accentuation of the texture, in addition tothe clinical resolution, is an expression of theinvolvement of the lymphatics.

Aging and the Respiratory System 697

Pleural effusion concerns the systemic circula-tion and requires the failure of the right heart, dif-ferent from pulmonary edema. This means thatthe mechanism of formation of pleural effusionhemodynamically requires conditions differentfrom those for pulmonary edema and therefore, al-though nearly always present, is a complimentarysign of it (Fig. 16B) (phase III).

From phase IV, dyspnea appears with minimumeffort, with a tendency to hypoxia at rest. The pa-tient is therefore not able to lie in a supine positionbut tends to be seated to facilitate the activity ofthe respiratory muscles. CT clarifies dyspnea andpostural worsening of hypoxia: if, in the non-com-pensated cardiopathic patient, a densitometricmeasurement is made of the pulmonary paren-chyma, with the placement of a region of interest(ROI) at the level of the pulmonary mantle dorsallyand ventrally, the densitometric gradient is re-duced or eliminated (Fig. 18). This occurs becauseperfusion does not prevail in the lung’s dorsalareas, as normally occurs in individuals in a supineposition, but is increased, also ventrally, whereventilation should prevail, because of recruitmentof the ‘‘reserve’’ pulmonary vascular area. This re-sults in elimination of the densitometric gradientor, in physiopathologic terms, in the creation ofa ventilation/perfusion discrepancy, the cause ofhypoxia and dyspnea. In conclusion, the patientwho has cardiogenic failure needs to assume anorthopneic position to restore the densitometricgradient, and an acceptable ventilation/perfusionrelationship.28

‘‘Pulmonary Heart’’

COPD is the second most frequent cause of in-validity, hospitalization, and death of the elderly

Fig. 18. Dorsal/ventral pulmonary densitometric gradientgradient of approximately 50 UH between region of intedo not show a densitometric gradient between the two ROdent areas.

in the pneumologic context, and is three to fivetimes more frequent at this age than at otherages.44

In such cases, the involutive aspects of the lung,as described previously, prevail and result ingreater air content and hence, hyperdistension.The hyperexpanded lungs reduce the space avail-able to the heart, particularly in the diastole, andalmost ‘‘imprison’’ it, giving it a median or a vertical‘‘drop’’ appearance (Fig. 19), which is the model ofthe PH.16,22

‘‘Cardiac lung’’ versus ‘‘pulmonary heart’’The CL and PH physiopathologic models are op-posites and specular images, equidistant fromthe normal. Comparison is therefore useful for bet-ter understanding. In Table 2, the radiologic, phys-iopathologic, and clinical aspects of the twomodels are listed.

The CL begins with left cardiopathy, including, inrapid succession, cardiomegaly, pulmonary ve-nous hypertension, non-compensated left cardi-opathy, and reduction of pulmonary volumes dueto the cardiomegaly.41,42 The PH almost alwaysbegins with COPD, which results in an increasein vascular resistance (ie, peripheral pulmonary oli-gemia), pulmonary arterial hypertension, the ‘‘in-volvement’’ of the right heart, and the limitationof heart expansion by the hyperexpandedlungs.16,45–53

Thus, from the physiopathologic point of view, inthe case of the CL, the cardiomegaly results in theprogressive reduction of pulmonary volume, witha restrictive spirometric pattern (see Fig. 13). Inthe PH, the alterations of the airways result in pul-monary hyperdistension with an obstructive-typespirometric picture (see Fig. 19).

with CT. (A) Normal individual with densitometricrest (ROI) 1 and 2. (B) Individuals with CD underwayIs due to the presence of perfusion in the nondepen-

Fig. 19. Pulmonary heart. (A) Chest radiograph; (B) CT scan at the level of the pulmonary bases: the hyperex-panded lungs occupy more space than normal, limiting heart expansion, particularly in the diastolic refillingphase (clinical sign: tachycardia).

Bonomo et al698

The specular aspect of the densitometric mea-surements that can be obtained on CT examina-tion of the chest, as referred to earlier, shouldalso be noted. In both cases, the densitometric

Table 2Radiologic, physiopathologic, and clinical characteristics o

Cardiac L

Pulmonary

Radiology Physiopat

Left cardiomegalyYPulmonary volumesCT: elimination of the

dorsal/ventral gradient dueto perfusion prevalence

Left cardiPulmonarSpirometr/ Shunt

Pulmonary

COPD

Peripheral oligemia

[ Pulmonary volumesTransverse cardiac diameter YCT: elimination of the

dorsal/ventral gradient dueto ventilation prevalence

[ VascularPulmonary

hyperteninvolvemheart

Spirometry‘‘Dead spac

Developm

Cardiac lung

Almost rapid

Reversible anatomic/pathologicalterations

gradient is eliminated. In the CL, this eliminationis produced by an abnormal increase of perfu-sion in the lung’s ventral areas, whereas in thePH, it is attributable to an abnormal increase in

f the ‘‘pulmonary heart’’ versus the ‘‘cardiac lung’’

ung

edema

hology Clinically

ac insufficiencyy venous hypertensiony / restrictive patterneffect

TachypneaAcute onset

heart

resistancearterialsion andent of the right

/ obstructive patterne’’ effect

TachycardiaChronic onset

ent

Pulmonary heart

Slow or stable

Irreversible anatomic/pathologic alterations

Aging and the Respiratory System 699

ventilation of the dorsal areas. Thus, in the CL,the density moves toward higher values, whereasin the PH, it moves toward lower values. In bothcases, a ventilation/perfusion deficit is created,responsible for hypoxemia and posturaldyspnea.28,46

The foregoing correlates perfectly with thephysiopathologic concepts according to which,when perfusion prevails, as in the case of the CL,there is a ‘‘shunt’’ effect, whereas, when ventila-tion prevails, as in the case of the PH, there isa ‘‘dead space’’ effect.46,47

From the clinical point of view, the distinctivesign of the CL is tachypnea, whereas that of thePH is tachycardia, both of which may progressto dyspnea. In the first case, a reduction of pulmo-nary volume subsequent to cardiomegaly resultsin the need to compensate for the deficit with anincreased number of respiratory acts; in the sec-ond case, the pulmonary hyperexpansion hindersparticularly the cardiac diastole (ie, ventricularrefilling, often of the left ventricle) and results inan increased number of cycles.46

Separating the left and right sections of the heartand arterial and venous microcirculation of thelungs makes it easier to understand the specularphysiopathology of the two models. The CL, orig-inating in the left cardiac cavity, involves, in a retro-grade manner, the pulmonary venous circulation;the PH, beginning in the arterial section of pulmo-nary microcirculation, involves the right cardiaccavity.22,28

The temporal aspect (ie, the time necessaryfor the conditions to become manifest) alsoemphasizes the mirror-like aspect of the twomodels. The CL, clinically expressed by pulmo-nary edema, establishes itself and develops rap-idly, tumultuously, and sometimes dramatically,showing extremely variable radiologic picturesfrom day to day, insofar as the pathology is acuteand the anatomic/pathologic aspects are revers-ible. The PH, clinically expressed by COPD,develops slowly, with essentially stabilized radio-logic pictures (apart from superimposed acuteepisodes) because the disease is chronic andthe anatomic/pathologic alterations areirreversible.47

The symptom common to the CL and the PH(dyspnea) also unites them in an significant aspectof the chest radiograph: the radiographs are takenin shallow inspiratory apnea, not because of insuf-ficient patient cooperation or poor test quality, butbecause of reduced inspiratory capacity, as gen-erally occurs in the elderly (above and beyondthe two models proposed) because of the involu-tion of the osteomuscular portion of the thoraciccage.4,6

TECHNICAL ANDMETHODOLOGICCONSIDERATIONS

No single technique perfectly reveals all the chestcomponents, but techniques exist that, together,constitute the best possible compromise, giventhe various, often contrasting, requirements. Thelatitude of the system, however broad, does notenable optimal simultaneous visualization of thoseareas with low radiant beam absorption, the lungs,and those with high absorption, the mediastinum.4

In the young and the adult, a complete visualiza-tion of the pulmonary fields, showing the ‘‘blindareas,’’ is a priority because of the predominantclinical need to detect focal pulmonary lesions. Inthe elderly, on the other hand, it is above all impor-tant to assess the pulmonary and cardiac circula-tion because the principal causes of invalidity,hospitalization, and death are cardiovasculardiseases.

Performing chest radiographs and preoperativetests in young, apparently healthy, individuals maygive rise to doubts about use and costs; con-versely they are essential in geriatric age, insofaras they immediately and reliably study vital, funda-mental parameters in individuals often affected bymultiple pathologies characterized by largely unre-solved clinical semiotics.2

Given that the earliest radiologic sign of pulmo-nary circulation overload (ie, redistribution of theflow, which makes it possible to detect this hemo-dynamic anomaly in the preclinical phase) may notbe visible in the elderly patient because of thefrequent presentation of the ‘‘dirty chest,’’ it be-comes indispensable to increase to the maximumthe value of the second sign, that is, the shadedaspect of the pulmonary picture caused by anincrease in extravascular fluid, particularly if thechest radiograph has not been performed understandard conditions.31

If this second sign was not accessible or provedequivocal, it would present a risk for further delayin the radiologic diagnosis or, even worse, ofreferring it to the clinician in a phase of evidentdecompensation.20

The technique performed must therefore givepriority to the gray pulmonary background, anexpression of the extravascular interstitial com-partment, and the contrast must not becompromised.4

High-voltage techniques compromise the con-trast, because their purpose is to identify betterthe ‘‘blind’’ pulmonary areas (retrocardiac, para-vertebral, and so forth). Medium-voltage tech-niques, on the other hand, are better suited tothe clinical necessities of the elderly. Having lessrecording latitude, they may not identify small focal

Bonomo et al700

lesions but, instead, valorize all aspects of the pul-monary circulation, which is of greater interest.

In the elderly, technically limited radiologicexaminations are the norm (ie, those done witha single anterior/posterior projection with the pa-tient seated or supine) precisely because the signsof cardiovascular disease that must be examinedwith radiograph are also the primary cause ofinvalidity. For this reason, it is essential to valorizethose few most meaningful aspects that chestradiographs done under these conditions, particu-larly the shaded aspect of the hilar/pulmonaryvascular structure contours, make possible toevaluate.2,11

THE RADIOLOGIC REPORT

Although the acquisition of images is delegated,for the most part, to the radiology technician, thewriting of the report is the sole responsibility ofthe radiologist who, in so doing, performs theclinical role of specialist.54

The report is the main means of communicationwith the requesting physician and its effectivenessis measured on the basis of its usefulness inclarifying the patient’s clinical problems. Themore a report influences diagnosis and treatment,the more it will be truly useful and the more theradiologist will have been able to actprofessionally.

To formulate a good report, the radiologist musthave a good understanding of the clinical questionand must adhere to certain basic rules of communi-cation, summarized by Bonmati and colleagues asthe six ‘‘c’s’’: clear, correct, concise, complete, co-herent, andcompetent, towhich a further ‘‘c’’ shouldbe added: common (in the sense of ‘‘shared’’).55,56

In fact, if the radiologist is not on the same wave-length as the person requesting the report (ie, if he/she does not take into consideration what thelatter wants and whether or not the languageused in the report will be understood), then thisis a failure of communication. Thus, if the reporton the chest radiograph in Fig. 13 uses the expres-sion ‘‘type 1:1 vascular distribution’’ withoutexplaining the clinical meaning (occupation of the‘‘reserve’’ vascular area as the first sign of venousoverload of the pulmonary circulation), it may wellbe technically exemplary but clinically ineffective,because it is not a given that this expression willbe understood by the requesting physician.

Further, in a study of the heart by means of chestradiograph, the signs may be numerous andshould be listed in the report, because they arepart of classic radiologic semeiotics. If theyare not translated into clinical terms, however,a comprehensive picture is not provided, which

presents a risk that the report will be nothingmore than a useless academic exercise. Thus,a competent report is produced but it is neitherclear nor clinically effective.

A great deal has been, and is still being, dis-cussed regarding the conciseness of the report,even more today, with the availability of testsreplete with images, such as multidetector CT,and with details, such as chest radiograph withdigital technique. The radiologist must not merelydescribe the findings but must also interpretthem, expressing a professional opinion in theform of a diagnostic conclusion, if the intent is tohave an influence on the patient’s clinical course.

Thus, in conclusion, the report must be com-plete and must have a precise structure: clinicalquestion, description of findings, diagnostic judg-ment, any indications for the performing of thediagnostic procedure, and so forth.57

In the elderly, then, basic knowledge of cardio-respiratory physiopathology is essential. For ex-ample, if, in the initial CD, pulmonary fields areunderexpanded on inspiration, this is not becausethe patient is less cooperative but because thelungs are less compliant, which must be pointedout in the report.

The radiologist must always bear in mind theclinical requirements and, given the possibility ofcardiopathy (above and beyond the presence orabsence of focal lesions), must describe the con-ditions of the pulmonary circulation, particularlyin the initial stages of CD, because this is themost important information for the clinician and,in these phases, the diagnosis of CD may be radio-logic only. In subsequent phases, when CD be-comes clinically evident, the radiologist needonly monitor the clinical picture, particularly theextravascular pulmonary water and thecardiomegaly.

Hence, to be effective, the radiologist must givethe chest radiograph examination a hemodynamicreading, always describing in the report the condi-tions of the pulmonary circulation, particularly if itis altered. A description of the normality of distri-bution and clarity of the contours and assessmentof the appearance of the pulmonary circulation inrelationship to the cardiac morphology shouldalso be included. If the heart is large, it is morelikely that the pulmonary circulation will not bealtered.57

SUMMARY

In the elderly, the chest without evident pathologyis characterized by findings that occupy a sortof ‘‘no man’s land’’ between the normal andthe pathologic. Aging results in physiologic

Aging and the Respiratory System 701

modifications that must be recognized so as not tobe interpreted erroneously as pathologies. On theother hand, the elderly tend to become ill more fre-quently and multipathologies are more frequent.Image diagnostics is a key element in the clarifica-tion of often blurry clinical pictures, which maymake early diagnosis possible, a great advantageto timely treatment. In this sense, knowledge ofheart/lung interactions makes it possible to obtain,from the onset, radiologic and clinical signs ofthe two physiopathologic models prevalent in theelderly, the ‘‘cardiac lung’’ and the ‘‘pulmonaryheart.’’

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