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In the new classification system Table 23-1, PPH is one of a group of entities that share common clinical and pathological presentations included under the broader heading of pulmonary a

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of the pulmonary artery in four patients, esophagus in

one, and main stem bronchus in one other patient There

were no operative deaths, and most patients were

asymp-tomatic at follow-up

The role of therapeutic bronchoscopy remains

contro-versial In the series by Cole and colleagues, of 42 patients

with broncholithiasis, bronchoscopy was performed in

40, with successful stone removal achieved in 8 (20%).43

Cole and colleagues recommended that, while removing

bronchial stones, excess force or traction should be

avoided and that the use of bronchial irrigation may help

to separate the stone from the bronchial wall They also

concluded that an attempt at endoscopic stone removal

should be undertaken before complications develop

In the absence of significant symptoms or

complica-tions, observation alone may be the best management

strategy

References

1 Laennec RT A treatise on diseases of the chest and mediate

ausculation 4th ed Translated by J Forbes New York: S.

Woodsons; 1835 p 100.

2 Kutlay H, Cangir AK, Enön S, et al Surgical treatment in

bronchiectasis: analysis of 166 cases Eur J Cardiothorac

Surg 2002;21:634–7.

3 Sealy WC, Bradham RR, Young WG The surgical treatment

of multisegmental and localized bronchiectasis Surg Gynec

6 Heller G Beitrage zur lehre van den fremdkorpern in den

luftwegen Göttingen: WF Kaestner; 1890.

7 Kartagener M Zur pathogenese der bronchiectasien.

Bronchiectasien bei situs inversus viscerum Beitr Klin

Tuberk 1933;8:489–501.

8 Heidenhain L Ausgedehnte lungenresektion wegen

zahlmeicher eiternder bronchiectasien in einem

unter-lapen, verlandl.deutsch gesselsch Chir 1901;30:636.

9 Jackson C The bronchial tree: its study by the insufflation of

opaque substances in the lung Am J Roentgenol 1918;5:454.

10 Sicard JA, Forestier J Iodized oil as contrast medium

radioscopy Bull Mem Med Hôp de Paris 1922;46:463.

11 Brock RC Post-tuberculous bronchostenosis and

bronchiectasis of the right middle lobe Thorax 1950;5:5.

12 Wager KB, Johnston MR Middle lobe syndrome Ann

Thorac Surg 1983;35:679–86.

13 Saha SP, Mayo P, Lang GA, McElvein RB Middle lobe

syndrome: diagnosis and management Ann Thorac Surg

17 Ashour M, Al-Kattan K, Rafay MA, et al Current surgical therapy for bronchiectasis World J Surg 1999;23:1096–104.

18 Nicotra MB, Rivera M, Dale AM, et al Clinical, ologic, and microbiologic characterization of bronchiecta- sis in an aging cohort Chest 1995;108:955–61.

pathophysi-19 Davis AL, Pierce AK, Naidich D, et al Bronchiectasis Am Rev Respir Dis 1986;134:824–5.

20 Eliasson R, Mossberg B, Canner P, Afzelius BA The immobile-celia syndrome A congenital ciliary abnormality

as an etiologic factor in chronic airway infection and male sterility N Engl J Med 1977;297:1–6.

21 Smit HLM, Schreurs JM, Van den Bosch JMM, Westermann CJJ Is resection of bronchiectasis beneficial in patients with primary ciliary dyskinesia Chest 1996;109:1541–4.

22 Tkebuchrava T, Neiderhauser U, Weder W, et al Kartagener’s syndrome Clinical presentation and cardio- surgical aspects Ann Thorac Surg 1996;62:1474–9.

23 Vevaina JR, Teichberg S, Buschman D, Kirkpatrick CH Correlation of absent inner dyneic arms and mucociliary clearance in a patient with Kartagener’s syndrome Chest 1987;91:91–5.

24 Wayne KS, Taussig LM Probable familial congenital bronchiectasis due to cartilage deficiency (Williams- Campbell syndrome) Am Rev Respir Dis 1976;114:15–22.

25 Mounier-Kuhn P Dilatation de la trachée: constatations radiographiques et bronchoscopiques Lyons Med 1932;150:106–9.

26 James DK, Godden D, Cavanagh P Alpha-1-antitrypsin deficiency presenting as bronchiectasis Br J Dis Chest 1985;79:301–4.

27 Grenier P, Maurice F, Mussel D, et al Bronchiectasis: ment by thin-section CT Radiology 1986;161:95–9.

assess-28 Muller NL, Begin CJ, Ostrow DN, Nichols DM Role of computed tomography in the recognition of bronchiectasis.

Am J Radiol 1984;143:971–6.

29 Kang EY, Miller RR, Müller N Bronchiectasis: comparison

of preoperative thin-section CT and pathologic findings in resected specimens Radiology 1995;195:649–54.

30 Cooke JC, Currie DC, Morgan AD, et al Role of computed tomography in the diagnosis of bronchiectasis Thorax 1987;42:272–7.

31 Munro NC, Cooke JC, Currie DC, et al Comparison of thin-section computed tomography with bronchography for identifying bronchiectatic segments in patients with chronic sputum production Thorax 1990;45:135–9.

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32 Chipps BE, Talamo RC, Winkelstein JA IgA deficiency,

recurrent pneumonias, and bronchiectasis Chest

1978;73:519–26.

33 Ellis DA, Thornley PE, Wrightman AJ, et al Present outlook

in bronchiectasis: clinical and social study and review of

factors influencing prognosis Thorax 1981;36:659–64.

34 Jaffe HJ, Katz S Current ideas about bronchiectasis Am

Fam Physician 1973;7:69–76.

35 Hodder RV, Cameron R, Todd TRJ Bacterial infections In:

Pearson FG, et al, eds Thoracic surgery New York:

Churchill Livingstone: 1995 p 433–70.

36 Mazières J, Murris M, Didier A, et al Limited operation for

severe multisegmental bilateral bronchiectasis Ann Thorac

Surg 2003;75:382–7.

37 Barlow CW, Robbins RC, Moon MR, et al Heart-lung

versus double-lung transplantation for suppurative lung

disease J Thorac Cardiovasc Surg 2000;119:466–76.

38 Agasthian T, Deschamps C, Trastek VF, et al Surgical

management of bronchiectasis Ann Thorac Surg

1996;62:976–80.

39 Ripe E Bronchiectasis Scand J Respir Dis 1971;52:96–112.

40 Fujimoto T, Hillejan L, Stamatis G Current strategy for

surgical management of bronchiectasis Ann Thorac Surg

2001;72:1711–5.

41 Deslauriers J, Dion L Le traitment des bronchiectasies primitives Indications chirurgicales et resultats Semin Hôp Paris 1985;18:1199–201.

42 Faber LP, Jensik RJ, Chawla SK, Kittle CF The surgical implication of broncholithiasis J Thorac Cardiovasc Surg 1975;70:779–89.

43 Cole FH, Cole FH Jr, Kandedar A, Watson DC Management of broncholithiasis: is thoracotomy necessary? Ann Thorac Surg 1986;42:255–7.

44 Schwartz J, Schaen MD, Picardi JL Complications of the arrested primar y histoplasmic complex JAMA 1976;236:1157–61.

45 Dixon GF, Donnenberg RL, Schonfeld SA, Whitcomb ME Clinical commentary Advances in the diagnosis and treat- ment of broncholithiasis Am Rev Respir Dis 1984;129:1028–30.

46 Kowal LE, Goodman LR, Zarro VJ, et al CT diagnosis of broncholithiasis J Comput Assist Tomogr 1983;7:21–3.

47 Trastek VF, Pairolero PC, Ceithame EL, et al Surgical management of broncholithiasis J Thorac Cardiovasc Surg 1985;90:842–8.

48 Potaris K, Miller DL, Trastek VF, et al Role of surgical resection in broncholithiasis Ann Thorac Surg 2000;70:248–52.

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ROBERT M WINSLOW,MD

Blood substitutes are solutions that are intended to be

used instead of blood In fact, there are many “blood

substitutes” in clinical use now, including colloids and

crystalloids, which are given to perform one function of

transfused blood: plasma volume expansion However, the

term “blood substitutes” is usually reserved for solutions

that also carry and deliver oxygen Various workers in the

field of blood substitutes research have used other terms

to more accurately describe these new solutions, including

“oxygen carriers,” “oxygen-carrying plasma expanders,” or,

in reference to those solutions based on hemoglobin,

“hemoglobin-based oxygen carriers.” Although

perfluorocarbon-based oxygen carriers also have been

tested extensively, as a class they have limitations that have

slowed development In this chapter, main emphasis is

placed on hemoglobin-based products, since they hold

the most promise for successful clinical application

The search for alternatives to blood transfusion is

almost as old as the practice of medicine itself.1Prior to

the discovery of blood types, around 1900, and the

intro-duction of blood banks, just prior to the outbreak of

World War II, there was no effective replacement for

blood lost in hemorrhage Great efforts have been

invested in alternatives to products based on

hemoglo-bin, such as the perfluorocarbons Perfluorocarbons are

synthetic materials that have greatly increased solubility

for O2 and that can be produced cheaply and in large

volume They suffer from two significant problems,

however: they are completely immiscible with aqueous

solutions and so must be emulsified prior to infusion,

and under normal circumstances they cannot transport

sufficient O2to effectively oxygenate tissue Clinical trials

have not been convincing,2and no product is currently

approved for use in patients

Other more exotic solutions to the blood substituteproblem have been devised, including artificial red cells(liposomes)3and a variety of approaches based onrecombinant hemoglobins.4However, the products thathave been most successful in clinical development to datehave been chemical modifications of either human oranimal (cow) hemoglobin.5

Historical Background

In 1949 Amberson published a landmark paper thatdescribed a case report of a 22-year-old female withsevere postpartum hemorrhage as a result of retainedplacenta (Figure 22-1).6Her hemoglobin was 5 g/dL, andall compatible blood in the hospital had been exhausted.She remained in shock, and her blood pressure was notresponsive to conventional plasma expanders or crystal-loids She was finally given an experimental hemoglobin-saline solution that Amberson had been developing inthe laboratory Upon administration of this solution, theblood pressure rose dramatically and the heart rate fell.Over two liters of hemoglobin solution were adminis-tered to this patient, and for a time she seemed toimprove Eventually however her urine output dimin-ished as renal failure progressed and she finally died

In his discussion of this case, Amberson expressed hisbelief that the hemoglobin solution had been effectivetreatment for shock However, he cautioned that theblood pressure responses and the abrupt fall in heart ratewere peculiar properties of hemoglobin solutions, and hefelt that these effects were most likely owing to impuri-ties Amberson concluded, “It must be emphasized thatevery investigator in this field has used a differentmethod for the preparation of his hemoglobin-saline

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However the blood pressure responses after resuscitation

with either purified hemoglobin (Ao) or -Hb was a

marked overshoot compared with baseline, and both

hemoglobin solutions caused a modest reduction of

hear t rate relative to baseline, consistent w ith

Amberson’s earlier observations (see Figure 22-1)

Although volume restitution was the same with all the

solutions, the cardiac output failed to return even to

baseline with either hemoglobin solution In contrast,

cardiac output rose to levels even higher than baseline

after resuscitation with either albumin or Ringer’s

lactate The result of these physiological changes was a

marked increase in systemic vascular resistance

(Resistance = Pressure/Flow) after resuscitation with any

hemoglobin solution Finally, this increased resistance

completely offset any added O2-carrying capacity

afforded by infusion of hemoglobin solution

In summary, the US Army had succeeded in ing a suitable model hemoglobin that had the aimed-forcharacteristics:

produc-• is sterile

• is free of red cell membranes

• is endotoxin-free

• does not dissociate into  subunits

• does not cause significant renal toxicityNevertheless,-Hb still caused significant hyperten-sion in pigs Of even more concern, however, was the factthat cardiac output was depressed, presumably because ofintense vasoconstriction, as evidenced by severelyincreased vascular resistance The overall conclusion wasthat there was no advantage of resuscitation with -Hbcompared with Ringer’s lactate The mechanism of thisvasoactivity was not clear, and the Army concluded thatmore basic research was needed in the field in order to

Albumin Ao RL aaHb

Heart Rate

120 130 140 150 160 170 180 190 200

FIGURE 22-2 Simulation of a battlefield injury by the US Army Dehydrated pigs were subjected to hemorrhage (arrow at 0 hours) and then

resuscitated with test solution (arrow at 1 hour) The pattern of increased pressure, decreased cardiac output, and markedly elevated vascular resistance is the hallmark reaction to first-generation hemoglobin-based blood substitutes 15

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produce a safe and efficacious blood substitute The

Army not only abandoned -Hb as an experimental

product but discontinued further research in the field as

well.16Baxter continued to develop -Hb until phase III

clinical trials in stroke17and trauma18showed increased

mortality in treated patients

Vasoconstriction and Its Physiological Basis

The focus of research efforts in the post-Army era became

understanding of the mechanism of

hemoglobin-induced vasoconstriction Experiments carried on the

hamster skinfold model of the microcirculation led to

new insight into the cause of hypertension Figure 22-3

shows a study of functional capillary density, defined as

the number of capillaries in a given microscopic field in

which cells can be observed to be moving Functional

capillary density decreases when precapillary arterioles

constrict Thus, if blood volume does not change,

arteri-olar vasoconstriction produces hypertension and

decreased functional capillary density.19

In the experiment in Figure 22-3, animals were

progressively hemodiluted with dextran or hemoglobin

solutions When the hematocrit fell below 20% and

plasma hemoglobin concentration increased, functional

capillary density fell rapidly In contrast to this normal

response, when animals were progressively hemodiluted

with -Hb, the drop in functional capillary density

occurred at a much higher hematocrit, directly

demon-strating the marked vasoactivity of this product A

poly-merized human hemoglobin demonstrated this effect to

a lesser degree, and a hemoglobin modified by surface

decoration with polyethylene glycol (PEG) was even less

vasoactive These experiments suggested that not all

hemoglobin solutions are equally vasoactive

In rats, hypertension produced by these three types ofmodified hemoglobins was directly correlated with thefall in functional capillary density observed in hamsters(Figure 22-4) That is, PEG-modified hemoglobin had nosignificant effect on rat blood pressure, polymerizedhemoglobin had a small effect, and cross-linked hemo-globin was markedly hypertensive

Thus, in the early 1990s products from all classes ofmodified hemoglobins were entering advanced clinicaltrials in humans, but there was still no good explanationfor the hemodynamic pattern observed more than 40years previously One potential explanation seemed obvi-ous when NO was identified as an endothelial-derivedrelaxing factor.20 Hemoglobin was well known to bind

NO with high affinity,21and experiments with isolatedvascular rings seemed to support this explanation.22Oneproblem with this as a complete explanation, however,was that hemoglobin within red blood cells also binds

NO, but without a hypertensive effect A second problemwas that different modified hemoglobins demonstratedhypertension to differing degrees, depending on the type

of chemical modification (see, for example, Figure 22-4)

A New Model for Blood Substitute

Design

A problem with this interpretation, however, is that thereactivity with NO does not correlate with the degree ofvasoactivity Rohlfs and colleagues prepared solutions ofmodified hemoglobins with differences in molecular sizeand other significant properties (Table 22-1).24The cross-linked hemoglobin was the Army’s -Hb, with a molec-

Crosslinked PEG

30 40 50

60

FIGURE 22-3 Functional capillary density (FCD) as a function of

hema-tocrit in the hamster skinfold model with progressive hemodilution

with the indicated solutions Data for dextran and -Hb are from Tsai

A et al (1995) 19 Data for PEG-Hb and polymerized hemoglobin are

unpublished (personal communication, A Tsai and M Intaglietta,).

160

Polymerized Crosslinked PEG

60

FIGURE 22-4 Blood pressure in the rat in response to infusion of test

“blood substitutes.” Table 22-1 gives the properties of the test tions Infusion is via a femoral vein, starting at 30 minutes as shown

solu-by the arrow Note that the degree of blood pressure elevation is inversely proportional to functional capillary density, as shown in Figure 22-3 (unpublished data).

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The test of any design has to be in animals and then

humans In anticipation of clinical trials, rats were

exchange-transfused 50% of their blood volume and

then subjected to a 60% hemorrhage over 1 hour.32The

result of this study was that animals exchanged with a

new experimental PEG-modified human hemoglobin

survived the hemorrhage, while 50% of the control

subjects (no exchange) and animals exchanged with

either cross-linked or polymerized hemoglobins did not

(Figure 22-5) A striking feature of this experiment was

the difference in hemoglobin concentrations in the

vari-ous groups of animals The controls had a hemoglobin of

13.8 g/dL, while the PEG-Hb animals began the

hemor-rhage with a hemoglobin of only 7.6 g/dL According to

conventional clinical practice, these animals were at or

near the transfusion trigger at the beginning of

hemor-rhage These findings point to one of the most important

aspects of blood substitutes research and eventual clinical

use: “blood substitutes” are not simply blood

replace-ments but rather represent an entirely new category of

oxygen delivery therapy based on a new understanding of

oxygen transport physiology

Alternative Explanations for

Vasoconstriction

The theoretical basis for the success of PEG-modified

hemoglobin is not yet completely proven and remains

controversial Many workers in the field believe that NO

binding does account for hemoglobin-induced striction Recombinant hemoglobins with mutations thatreduce NO binding have been shown to cause less hyper-tension than native hemoglobin.33Others believe thatextravasation of hemoglobin is responsible, on the theorythat hemoglobin in the interstitial space more effectivelyscavenges NO than hemoglobin in the vascular space.34,35Some workers in the field have shown that vasoactivity isrelated to plasma viscosity36and that shear stress is trans-duced by endothelial cells to alter the release of vasoac-tive molecules such as NO and prostacyclins.37Still othersbelieve that vasoactivity or, more generally, toxicity,results from O2 free radical generation as hemoglobincycles through redox reactions.38It is possible, of course,that the final explanation may lie with a combination ofthese causative factors

vasocon-The Future of Blood Substitutes

Whatever the ultimate explanation for vasoactivityproduced by cell-free hemoglobin, it is very unlikely thatany product that is approved for clinical use will bearmuch resemblance to blood beyond its color It is veryunlikely that a hemoglobin-based red cell substitute can

be produced that has the same hemoglobin tion as normal red blood cells and the same oxygen affin-ity as red blood cells, with the same viscosity and oncoticpressure as human blood Nevertheless, as shown inFigure 22-5, solutions with properties very different fromthose of human blood can effectively reduce the need fortransfusion of allogeneic blood The problem for clinicalimplementation of such solutions, also demonstrated inFigure 22-5, is that the hemoglobin concentration per sewill no longer be a useful guide, or trigger, for giving atransfusion Rather, clinicians in the future must broadlyevaluate each patient’s need for supplemented tissue-oxygenating capacity and be prepared to administer thetherapy that best meets that need In this evaluationprocess, physiological and clinical data will need to beobtained and rapidly integrated into a reliable transfu-sion trigger As safer, more effective solutions are devel-oped for clinical testing, revision of the transfusiontrigger and definition of optimal clinical applicationsrepresent a major challenge for the developing field of

concentra-“blood substitutes.” As research and development withthese products continues, it is likely that the unique phys-iology of oxygen transport will be better understood, and

it should be possible to more effectively oxygenate tissuewhile reducing or avoiding allogeneic blood transfusion

0

7.6

13.8

6.8 11.0 10.2 Controls

FIGURE 22-5 Survival of rats after 50% exchange transfusion with

“blood substitutes” followed by hemorrhage of 60% of blood volume.

For properties of the hemoglobin solutions, see Table 22-1.

Pentastarch was used as an additional control because its viscosity

and oncotic pressure are similar to those of PEG-Hb The hemorrhage

starts at 0 minutes and takes place over 60 minutes The controls

represent a group of animals that were not exchange-transfused The

hemoglobin concentrations are the values measured at the start of

the hemorrhage 32

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1 Winslow R Hemoglobin-based red cell substitutes.

Baltimore (MD): Johns Hopkins University Press; 1992.

2 Gould S, Rosen A, Sehgal L, et al Fluosol-DA as a red-cell

substitute in acute anemia N Engl J Med 1986;314:1653–6.

3 Rudolph A Encapsulation of hemoglobin in liposomes In:

Winslow R, Vandegriff K, Intaglietta M, editors Blood

substitutes Physiological basis of efficacy New York:

Birkhaüser; 1995.

4 Looker D, Abbott-Brown D, Cozart P, et al A human

recombinant haemoglobin designed for use as a blood

substitute Nature 1992;356:258–60.

5 Stowell CP, Levin J, Spiess BD, Winslow RM Progress in the

development of RBC substitutes Transfusion

2001;41:287–99.

6 Amberson W, Jennings J, Rhodes C Clinical experience with

hemoglobin-saline solutions J Appl Physiol 1949;1:469–89.

7 Christensen S, Medina F, Winslow R, et al Preparation of

human hemoglobin Ao for possible use as a blood

substi-tute J Biochem Biophys Methods 1988;17:143–54.

8 Rabiner S, Helbert J, Lopas H, Friedman L Evaluation of

stroma-free haemoglobin for use as a plasma expander J

Exp Med 11967;26:1127–42.

9 Bunn H, Jandl J Renal handling of hemoglobin II.

Catabolism J Exp Med 1967;129:925–34.

10 Payne J Polymerization of proteins with glutaraldehyde.

Soluble molecular-weight markers Biochem J

1973;135:867–73.

11 Hsia J, Song D, Er S, et al Pharmacokinetic studies in the

rat on a o-raffinose polymerized human hemoglobin Artif

Cells Blood Substit Immobil Biotechnol 1992;20:587–95.

12 Chatterjee R, Welty E, Walder R, et al Isolation and

charac-terization of a new hemoglobin derivative crosslinked

between  chains (Lysine 991-Lysine 99 2) J Biol Chem

1986;261:9929–37.

13 Keipert PE, Gomez CL, Gonzales A, et al Diaspirin

cross-linked hemoglobin: tissue distribution and long-term

excretion after exchange transfusion J Lab Clin Med

1994;123:701–11.

14 Hess J, Macdonald V, Winslow R Dehydration and shock:

an animal model of hemorrhage and resuscitation of

battlefield injury Artif Cells Blood Substit Immobil

Biotechnol 1991;19:518.

15 Hess J, Macdonald V, Brinkley W Systemic and pulmonary

hypertension after resuscitation with cell-free hemoglobin.

J Appl Physiol 1993;74:1769–78.

16 Hess J, Riess R Resuscitation and the limited utility of the

present generation of blood substitutes Transf Med Rev

1996;10:276–85.

17 Saxena R, Wijnhoud AD, Carton H, et al Controlled safety

study of a hemoglobin-based oxygen carrier, DCLHb, in

acute ischemic stroke Stroke 1999;30:993–6.

18 Sloan EP, Koenigsberg M, Gens D, et al Diaspirin linked hemoglobin (DCLHb) in the treatment of severe traumatic hemorrhagic shock A randomized controlled efficacy trial JAMA 1999;282:1857–64.

cross-19 Tsai A, Kerger H, Intaglietta M Microcirculatory quences of blood substitution In: Winslow R, Vandegriff K, Intaglietta M, editors Blood substitutes Physiological basis

conse-of efficacy New York: Birkhäuser; 1995 p 143–54.

20 Ignarro L, Buga G, Wood K, et al Endothelium-derived relaxing factor produced and released from artery and vein

is nitric oxide Proc Natl Acad Sci U S A 1987;84:9265–9.

21 Gibson QH, Roughton FJW The kinetics and equilibria of the reactions of nitric oxide with sheep hemoglobin J Appl Physiol 1956;136:123–34.

22 Palmer R, Ferrige A, Moncada S Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor Nature 1987;327:524–6.

23 Vandegriff K, McCarthy M, Rohlfs R, Winslow R Colloid osmotic properties of modified hemoglobins: chemically cross-linked versus polyethylene glycol surface-conjugated Biophys Chem 1997;69:232–30.

24 Rohlfs RJ, Bruner E, Chiu A, et al Arterial blood pressure responses to cell-free hemoglobin solutions and the reac- tion with nitric oxide J Biol Chem 1998;273:12128–34.

25 Wittenberg J Myoglobin-facilitated oxygen diffusion: role

of myoglobin in oxygen entry into muscle Physiological Reviews 1970;50:559–636.

26 Lindbom L, Tuma R, Arfors K Influence of oxygen on perfusion capillary density and capillary red cell velocity in rabbit skeletal muscle Microvasc Res 1980;19:197–208.

27 Intaglietta M, Johnson P, Winslow R Microvascular and tissue oxygen distribution Cardiovasc Res 1996;32:632–43.

28 Vandegriff K, Winslow R A theoretical analysis of oxygen transport: a new strategy for the design of hemoglobin- based red cell substitutes In: Winslow R, Vandegriff K, Intaglietta M, editors Blood substitutes Physiological basis

of efficacy New York: Birkhäuser; 1995.

29 Winslow RM, Vandegriff KD Hemoglobin oxygen affinity and the design of red cell substitutes In: Winslow RM, Vandegriff KD, Intaglietta M, editors Advances in blood substitutes Industrial opportunities and medical chal- lenges Boston (MA): Birkhäuser; 1997 p 167–88.

30 McCarthy MR, Vandegriff KD, Winslow RM The role of facilitated diffusion in oxygen transport by cell-free hemo- globin: implications for the design of hemoglobin-based oxygen carriers Biophys Chem 2001;92:103–17.

31 Winslow RM, Gonzales A, Gonzales M, et al Vascular tance and the efficacy of red cell substitutes J Appl Physiol 1998;85:993–1003.

resis-32 Richmond KN, Shonat RD, Lynch RM, Johnson PC Critical PO(2) of skeletal muscle in vivo Am J Physiol 1999;277(5 Pt 2):H1831–40.

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33 Doherty DH, Doyle MP, Curry SR, et al Rate of reaction

with nitric oxide determines the hypertensive effect of

cell-free hemoglobin Nature Biotechnology 1998;16:672–6.

34 Baldwin AL Modified hemoglobins produce venular

interendothelial gaps and albumin leakage in the rat

mesentery Am J Physiol 1999;277(2 Pt 2):H650–9.

35 Bucci E Hemoglobin based oxygen carriers at a cross road:

the old paradigms must be abandoned and much more

basic science investigation is necessary [editorial] Artif

Cells Blood Substit Immobil Biotechnol 2001;29:vii–x.

36 Tsai AG, Friesenecker B, McCarthy M, et al Plasma ity regulates capillary perfusion during extreme hemodilu- tion in hamster skinfold model Am J Physiol (Heart Circ Physiol 44) 1998;275:H2170–H2180.

viscos-37 Frangos JA, Eskin SG, McIntire LV, Ives CL Flow effects on prostacyclin production in cultured human endothelial cells Science 1985;227:1477–9.

38 D’Agnillo F, Alayash AI Redox cycling of diaspirin linked hemoglobin induces G2/M arrest and apoptosis in cultured endothelial cells Blood 2001;98:3315–23.

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The first classification of pulmonary hypertension was

proposed at a World Health Organization (WHO)

symposium in 1973 Pulmonary hypertension was

classi-fied based upon etiologies with primary pulmonary

hypertension (PPH) classified as a separate class, that of

pulmonary hypertension of unknown etiology and

lack-ing associated clinical conditions PPH was further

subdivided into three groups based on pathology:

plexo-genic, recurrent thromboembolism, and veno-occlusive

disease Later it became apparent from epidemiological

data and the pathology of pulmonary hypertension that

no distinct pathological findings were pathopneumonic

for PPH, including lesions consistent with plexogenic

arteriopathy Epidemiological studies have demonstrated

a growing list of diagnoses that are associated with a

clin-ical condition and are indistinguishable from PPH

In 1998, the WHO convened a second symposium to

update the classification system of pulmonary

hyperten-sion and collate state-of-the-art understanding of

pul-monary hypertension

In the new classification system (Table 23-1), PPH is

one of a group of entities that share common clinical and

pathological presentations included under the broader

heading of pulmonary arterial hypertension (PAH).1

Four other classifications of pulmonary hypertension

include pulmonary venous hypertension, pulmonary

hypertension associated with disorders of the respiratory

system or hypoxemia, pulmonary hypertension due to

chronic thrombotic or embolic disease, and pulmonary

hypertension due to disorders directly affecting the

pulmonary vasculature

The WHO symposium of 1998 also provided a tional classification that is a modification of the New YorkHeart Association functional classification (Table 23-2)

func-Physiology and Pathobiology

Normally the pulmonary circulation is a low-pressure,high-flow vascular bed that has a remarkable capacity topermit increased cardiac output, such as exercise, withoutincreasing pulmonary arterial pressure The ability of thepulmonary vasculature to respond to increases in cardiacoutput is felt to be the result of the recruitment of under-perfused vessels and engorgement of highly capacitantvessels in response to increases in blood flow The physiol-ogy and histology of the pulmonary vasculature reflect thenormal state of affairs as the native smooth muscle tone ofpulmonary arterioles is lower and the smooth muscle layer

is thinner than that of the systemic circulation

Pulmonary arterial pressure is a function of the monary venous pressure, cardiac output, and pulmonaryvascular resistance (Table 23-3) The National Institutes

pul-of Health (NIH) Registry defined a normal meanpulmonary artery pressure at rest of 25 mm Hg, rising to

30 mm Hg with exercise.2A recent report of a series ofestimates of pulmonary arterial systolic pressure meas-ured by Doppler transthoracic echocardiography foundthat normal pulmonary artery pressures may be higherthan previously appreciated.3In this study of 3,790echocardiographically normal subjects, pulmonary arter-ial systolic pressure increased with age, body mass index,and sex Twenty-eight percent had pulmonary arterysystolic pressure > 30 mm Hg; it was suggested that theupper limit of normal may reach 40 mm Hg in olderpatients or obese patients

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pulmonary vascular tone.7Platelets, endothelial cells,

smooth muscle cells, and the extracellular matrix all are

important for the maintenance of normal vascular tone

Perturbations of the normal function of all these

ele-ments have been postulated to contribute to the

patho-logical changes of PAH Table 23-4 lists examples of cell

products and functions that contribute to normal

vascu-lar tone and alterations associated with PPH

Hypoxic vasoconstriction is the most important

phys-iological mechanism of pulmonary vasoconstriction The

mechanisms that lead to hypoxic vasoconstriction are

incompletely described Hypoxia at the level of the alveoli

causes local vasoconstriction, which is acutely reversible

by administration of oxygen If this phenomenon occurs

globally, then pulmonary hypertension results Chronic

states of hypoxia lead to vascular remodeling and result

in fixed increases in pulmonary vascular resistance

Hypoxia may further stimulate pulmonary hypertension

through the release of cytokines from the endothelial cell

Inflammatory cells may contribute as well through a

production of cytokines and growth factors Several of

the vasoactive compounds are also mitogens and may to

contribute to vascular remodeling

Endothelial cells are capable of producing a number

of vasoactive substances including vasodilators and

vaso-constrictors Abnormality in the metabolism of these

substances, favoring vasoconstriction, has been noted in

patients with PPH and in experimental animal models of

pulmonary hypertension Growth factors released from

the endothelial cell may stimulate to vascular remodeling

and alteration of the extracellular matrix

In the smooth muscle cells, much attention has been

placed upon the role of calcium and potassium channel

regulation K+channels regulate calcium influx into the

cell through a number of mechanisms Influx of calcium

into the smooth muscle cell leads to activation of the

contractile apparatus and vasoconstriction and possibly

initiates mitogenic effects as well Acute hypoxia triggers

pulmonary vasoconstriction at least in part by inhibitingone of the K+ channels found in pulmonary arterysmooth muscle cells

Vascular remodeling is a central feature of pulmonaryhypertension from all causes and has been used to bothclassify and grade the severity of pulmonary hyperten-sion Vascular remodeling includes changes in the intima(fibrosis, media, hypertrophy, and muscularization) andadventitia (increased deposition of extracellular matrix).Endothelial injury early in the course of PAH has beenhypothesized to permit exudation of factors that stimu-late smooth muscle cells to release mitogens such as basicfibroblast growth factor directly and adenosine indirectly.Membrane-bound metalloproteins and serine elastaseshave been postulated to be central in this process

The recent identification of mutations in the gene forbone morphogenetic protein receptor II in patients withfamilial PPH promises to provide insight into the patho-genesis of PPH.8,9 Bone morphogenetic protein receptor

II is a member of the transforming growth factor (TGF-) receptor family TGF- family of growth factorshave pleiotropic effects on endothelial cells, smoothmuscle cells, and fibroblasts The activities of the TGF-family are dependent upon the cellular milieu; they aremodified by complex cytokine networks in ways that may

be as divergent as promoting or inhibiting endothelialcell proliferation Thus, describing the common pathwaythat leads to PPH continues to present significant investi-gational challenges

Primary Pulmonary Hypertension

Primary pulmonary hypertension is a rare conditionwith an estimated annual incidence of one to two permillion people per year in Europe and the UnitedStates.6,10 However, this may be an underestimate, asautopsy studies have shown a prevalence of 1,300 permillion population The incidence of PPH rises drasti-cally among users of appetite suppressants to 25–50 per

TABLE 23-4 Examples of Pathogenetic Factors in Pulmonary Arterial Hypertension

EC = endothelial cell; ECM = extracellular matrix; MMP = matrix metalloproteinase; NO = nitric oxide; SMC = smooth muscle cell.

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million people per year.11The U.S NIH Registry

demon-strated that PPH can occur at any age and has a peak

incidence at 36 years The disease is more common in

females than males with a ratio of about 2:1 Familial

cases of PPH were noted in the registry This observation

led to further understanding of the genetic basis of PPH

(see below) Familial PPH occurs in approximately 10%

of cases There is no association between race and PPH

There is a spectrum of clinical signs and symptoms

that occur at presentation in PPH (Table 23-5) The most

common presentation, however, is the insidious onset

and progression of dyspnea on exertion The nonspecific

nature of the presentation led to a delay in diagnosis on

an average of 2 years in the NIH Registry

Physical findings may suggest the diagnosis Most

commonly noted are an accentuated second heart sound

and a right ventricular S4 As the condition worsens, the

right ventricle becomes hypertrophied, which leads to a

right ventricular heave and tricuspid regurgitation

Dilatation of the annulus of the pulmonary valve or right

ventricle outflow track leads to a murmur of pulmonic

regurgitation A right ventricular S3 gallop occurs with

right ventricular failure and is an ominous sign,

associ-ated with decreased cardiac output and increased right

atrial pressures

The diagnosis of PPH is a diagnosis of exclusion

Following the recommendations and experience gained

from the NIH Registry open lung biopsy is no longer

recommended for the diagnosis of PPH

Quite often, patients will have had a series of tests to

evaluate their dyspnea prior to the diagnosis of pulmonary

hypertension Typically, these tests include pulmonary

function tests, which may be normal or demonstrate early

restrictive disease (which may become prominent in severe

PPH) and mild to moderate impairment of the diffusing

capacity The chest radiograph commonly shows large

pulmonary arteries (Figure 23-1).12The right pulmonary

interlobar artery is considered enlarged when it is 16 mm

or greater in men and 15 mm or greater in women With

enlargement, the left main pulmonary artery causes a

convexity under the aortic arch Pulmonary function tests

and chest radiograph are of assistance also in ruling outsignificant pulmonary airway or parenchymal diseases asthe cause of the dyspnea

The initial evaluation of the pulmonary ics is best made by echocardiography Transthoracicechocardiography can characterize the shape and size ofthe chambers and identify hypertrophy of the right

hemodynam-TABLE 23-5 Prevalence of Symptoms of Primary

FIGURE 23-1 Young woman with primary pulmonary hypertension

associated with anorexigen use A, Chest radiograph demonstrates mild cardiomegaly, enlargement of the interlobar artery (small arrow),

and convexity resulting from enlargement of the left main pulmonary

artery (large arrow) B, Chest computed tomography scan

demon-strates normal pulmonary parenchyma and confirms that cardiomegaly is due to right ventricular enlargement.

A

B

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ventricle Decreased filling of the left ventricle may be

noted, as may paradoxical movement of the

intraventric-ular septum towards the left ventricle Doppler

echocar-diography can be used to estimate the pulmonary arterial

systolic pressure This is done by measuring systolic flow

velocity across pulmonic valve or, more accurately, by

regurgitant flow across the tricuspid valve.3The

echocar-diogram is also useful in ruling out intracardiac shunts,

which cause high flow states and secondary pulmonary

hypertension Small shunts are best demonstrated by

transesophageal echocardiography

Once the diagnosis of pulmonary hypertension is

confirmed, associated medical conditions need to be

excluded Blood tests are obtained to screen for liver

disease, connective tissue diseases, and serology for

human immunodeficiency virus (HIV)-1 infection

Sufficient screening tests for connective tissue disorders

in patients who are otherwise asymptomatic include

antinuclear antibody, antineutrophil cytoplasmic

anti-body, rheumatoid factor, and an erythrocyte

sedimenta-tion rate A major category of disease that needs to be

excluded is thromboembolic disease Ventilation

perfu-sion scan or computed tomography (CT) angiography

can be used to exclude chronic thromboembolic disease

If chronic thromboembolic disease is suggested, then

pulmonary angiography should be performed to further

characterize the degree and distribution of the

throm-boembolic deficits.13Polysomnography is indicated if

there are clinical findings suggestive of sleep apnea.14

If testing rules out secondary causes of pulmonary

hypertension, the diagnosis of PPH can be made

However, further physiological evaluation is appropriate

In particular, cardiac catheterization is needed to fully

assess right ventricular and left ventricular

hemodynam-ics to confirm echocardiogram estimates of right

ventric-ular and pulmonary artery pressures and to further rule

out left-to-right shunts If risk factors for coronary artery

disease are present, the inclusion of coronary artery

angiography is useful as patients with PPH often present

with, or develop, atypical chest pain Cardiac

catheteriza-tion should include acute vasodilator testing Results

from the NIH Registry show that a positive response to

acute vasodilator test is predictive of clinical response to

oral vasodilatory agents A positive acute vasodilator test

is one in which there is a fall in the pulmonary artery

pressures of 20% or 10 mm Hg with either no change or

an increase in cardiac output.15

A 6-minute walk test provides important information

about the potential need for supplemental oxygen

ther-apy It is less time-consuming and expensive than a

formal cardiopulmonary stress test and is more easily

repeated for monitoring of response to therapy

Following the diagnosis of PPH and initiation of

ther-apy, transthoracic echocardiography can be used forsequential estimates of pulmonary artery systolic pres-sure to monitor response to therapy Follow-up with 6-minute walk tests is useful for ongoing titration ofsupplemental oxygen

The medical therapy of PPH has three aims The first

is vasodilation, the second is modulation of pulmonaryvascular remodeling, and the third is the prevention of insitu thrombosis

Vasodilator therapy is directed by the results of theacute vasodilatory test performed in the cardiac catheter-ization lab and the severity of pulmonary hypertensionupon presentation Historically, observations on the use

of multiple vasodilators identified that only a minority ofpatients would respond to these agents The responsivepatients are identified by the acute vasodilator test in thecardiac catheterization lab, and oral therapy with acalcium channel blocker is indicated The dosage should

be titrated to the maximal recommended dose if ated, avoiding systemic hypotension.16

toler-Intravenous infusion of epoprostenol (prostacyclin, orPGI2) has been shown to be efficacious even in patientswho do not have a positive acute vasodilator test.17In themajority of these patients, epoprostenol has been shown

to improve hemodynamics, increase exercise tolerance,and prolong survival Epoprostenol has the disadvantage

of a very short half-life of 3 to 5 minutes, requiringcontinuous intravenous infusions Administrationrequires an indwelling vascular catheter Meticulous care

of the catheter is essential, as line sepsis can quicklybecome life threatening in patients with fixed flowthrough their pulmonary vasculature Epoprostenol hasless worrisome side effects as well, including jaw pain (aclaudication-like pain relieved by chewing), headache,rash, diarrhea, and musculoskeletal pains, particularly inthe ankles and feet The dose of the drug is titrated toprovide for maximum exercise tolerance and is limited bydiscomfort from the minor side effects There is apparenttachyphylaxis to epoprostenol and dosing needs to becontinuously advanced to maintain efficacy

A newer alternative to epoprostenol is bosentan, aninhibitor of both the endothelin 1 and endothelin 2 recep-tors.18This drug has been demonstrated to improve hemo-dynamics and exercise tolerance in patients treatedfollowing the initial diagnosis of their PPH Long-termstudies documenting survival advantage are not yet avail-able Bosentan clearly has the advantage of not requiring acontinuous infusion, but liver toxicity and dose-dependent fall in hemoglobin require frequent monitoring.The possibility of switching patients from epoprostenol tobosentan has not yet been formally investigated Data toguide the selection of either epoprostenol or bosentanupon initial presentation do not yet exist Thus, one sug-

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gestion is that patients with class IV dyspnea on exertion

receive epoprostenol, reserving a trial of bosentan for

patients with class III dyspnea on exertion Other oral and

subcutaneous preparations are undergoing evaluation in

the United States or are available in Europe As these

become available, and until improvement in mortality is

documented, beginning patients with class IV dyspnea

on exertion on epoprostenol would remain a valid

recommendation

Care must be taken with the administration of any of

the vasodilators for PPH The sudden cessation of

vasodilator therapy may lead to rapid rebound in

pul-monary artery pressures, which can be life threatening

There is investigational evidence that both

epoprost-enol and bosentan have antimitogenic activities There

has also been some suggestion in the investigational

liter-ature that calcium channel blockers may have similar, if

not as potent, activities Thus, therapies with these

vasodilatory drugs also address the issue of vascular

remodeling Occasionally, patients do not show

improve-ment in their pulmonary artery pressures following

treat-ment with epoprostenol for up to 12 months This delay

in response supports the contention that the drug is

effecting vascular remodeling and is not acting merely as

a vasodilator

In situ thrombosis is an important complicating

feature of primary pulmonary hypertension

Non-randomized trials in which anticoagulation was initiated

with patients with abnormal ventilation–perfusion scans

but not in those with normal scans demonstrated a

survival advantage for patients receiving warfarin.16 On

the basis of these trials, the standard of care includes

anticoagulation with warfarin to maintain the

interna-tional normalized ratio (INR) between 2 and 3

The use of digoxin in patients with cor pulmonale is

controversial Some authorities recommend its use

because of its inotropic activity and reversal of the

neurohumoral activation that occurs with right heart

failure Diuretics should be used judiciously in patients

with cor pulmonale They are indicated for peripheral

edema associated with cor pulmonale or secondary to

high-dose calcium channel blockers Ascites can be a very

difficult complication of cor pulmonale to manage and

may respond to the addition of spironolactone to loop

diuretics Patients on diuretics must be closely monitored

for electrolyte abnormalities and to ensure that

intravas-cular volume is not depleted

Surgical approaches to PPH include atrial septostomy

This has been suggested for patients with severe

right-sided heart failure that is refractory to diuretics and in

patients with syncope resulting from poor filling of the

left ventricle The resulting right-to-left shunt leads to

decompression of the right ventricle and improved filling

of the left ventricle, but it is also associated with cant desaturation, which may not respond to oxygensupplementation

signifi-If medical therapy fails, then lung transplantation may

be a lifesaving intervention Single or double lung plants may be offered to patients with PPH Heart–lungtransplantation is generally reserved for patients withabnormal left ventricular function or congenital anom-alies Outcomes for lung transplantation for pulmonaryhypertension are slightly worse than for other diagnoses.Primarily this is because of higher morbidity and mortal-ity in the immediate postoperative period, which resultsfrom the stress placed upon the transplanted vascularbed by the hypertrophied right ventricle One and five-year survival rates are respectively 64 and 42%

trans-PPH tends to be a disease of young women Thus,pregnancy is a frequent issue in the care of these patients.Since patients with PPH have a cardiac output fixed bytheir abnormal pulmonary vasculature, the hemody-namic changes associated with pregnancy and the imme-diate postpartum period may be life threatening.Successful pregnancies with safe deliveries have beenreported, but contraception should be recommended as arule Oral contraceptives are contraindicated as they mayincrease the risk of deep venous thrombosis and pul-monary embolism

Prognosis for untreated PPH is poor with a meansurvival time of 212years in the NIH Registry.19Patientswho respond to oral vasodilation have a 95% 5-yearsur vival rate.1 6 The nonresponders treated withepoprostenol have significant improvement in theirsurvival rate as reflected by the fact that, in one study,91% of the patients with pulmonary hypertensionavoided listing for lung transplantation after initiation oftherapy.20

As listed in Table 23-1, ingestions and a number ofclinical conditions have been identified as probableetiologies for PAH Some such as HIV, portal hyperten-sion, and collagen vascular diseases are long-term condi-tions that have the potential to modify the pulmonaryvasculature on an ongoing basis Others, particularly thetoxic ingestions and use of weight-reduction aids, suggestthat PAH can be triggered by limited injury or exposure

It has been suggested that these short-term exposures,either by increasing shear forces or by direct stimulation,alter endothelial cell biology, which sets off a vicious,self-sustaining cycle of changes that eventuate in pul-monary arterial hypertension

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Chronic Thromboembolic Pulmonary

Hypertension

Chronic thromboembolic pulmonary hypertension

(CTPH) results as a rare sequela of pulmonary

embo-lism It accounts for a small fraction of patients who

survive acute pulmonary emboli, estimated at 0.1 to

0.5% Since pulmonary emboli can be an asymptomatic

event, the true incidence of patients with CTPH is not

known However, estimates place the total number in the

United States between 500 and 2,500 patients Patients

with CTPH can present with the insidious onset of

dysp-nea on exertion in a manner identical to the presentation

of PAH Since there is an effective surgical intervention

available, it is important to distinguish CTPH from other

causes of pulmonary hypertension.10

Acute pulmonary embolism rarely causes pulmonary

hypertension The exception occurs with massive acute

pulmonary embolism in which the embolus occludes

50% or more of the pulmonary vasculature in patients

with normal cardiopulmonary physiology or 30% for

patients with pulmonary or cardiac disease In patients

with massive pulmonary embolism, the risk of death is

greatest in the first few hours following the acute event

The vast majority of the patients who survive the first

few hours go on to have their embolus resolved within 3

weeks, with normalization of the pulmonary artery

pres-sures However, as noted above, in a minority of patients

resolution is incomplete Residual obstruction of 40% of

the pulmonary vasculature is associated with pulmonary

hypertension on the basis of the obstruction of large (ie,

main, lobar, or proximal segmental) arteries.21

Progres-sion of pulmonary hypertenProgres-sion occurs with recurrent

embolization or in situ thrombosis in the pulmonary

arteries Alternatively, progression of pulmonary

hyper-tension can occur as a result of vascular remodeling, with

pathological changes indistinguishable from those found

in pulmonary arterial hypertension In these cases,

pulmonary hypertension is out of proportion to the

degree of embolic obstruction of the pulmonary arteries,

hemodynamic worsening occurs without evidence of

recurrent thromboembolic events even in patients who

are fully anticoagulated, and, in cases where open

biop-sies were performed, the pathological changes of PAH in

the small distal arterioles were noted Only those patients

whose hemodynamic abnormalities are proportionate to

the degree of proximal arterial obstruction are candidates

for thromboembolectomy.10,22

As mentioned above, the presentation of patients with

CTPH is the same as with other forms of pulmonary

hypertension Dyspnea on exertion with insidious onset

and relentless worsening is the hallmark The other

symptoms, noted in Table 23-5, occur as the pulmonary

hypertension progresses On the whole, CTPH presentswith physical findings identical to PAH One distinguish-ing characteristic on physical exam is the finding ofbruits that are presumed to originate from turbulent flowthrough partially occluded pulmonary arteries in 30% ofpatients.23

The evaluation of patients with suspected CTPH issimilar to the evaluation of patients with PPH However,effort should be undertaken to assure that ongoing silentpulmonary embolism is not a continuing problem.Duplex scanning of the legs is noninvasive and indicated

in the clinic evaluation A large fraction of duplex scans

in patients with CTPH reveal evidence of prior venousthrombosis (35–45%) and are useful to rule out acuteactive thrombosis Patients should also be evaluated forcoagulopathies that put them at risk for recurrent emboliand failure of standard anticoagulation Up to 10% ofpatients have been found to have anticardiolipin anti-body.24,25Ventilation–perfusion scanning is often thestudy that provides the initial suspicion for CTPH Inpatients with CTPH, mismatched perfusion defects areseen usually at the segmental or larger levels However,ventilation–perfusion scans cannot be used to judge theextent of obstruction in thromboembolic disease.2 6Angiography, angioscopy, or surgery often shows moreextensive disease than that revealed by ventilation–perfusion scanning The role of CT angiography in theevaluations of patients with CTPH is undefined.Obstruction or partial obstruction of main, lobar, orsegmental arteries is common but is not yet felt to be asubstitute for angiography for defining the extent ofdisease

Right heart catheterization is indicated, as for PPH,for accurate hemodynamic characterization Pulmonaryangiography can be safely performed in patients withpulmonary hypertension but requires modifications ofstandard practices and careful monitoring and thusshould be performed in centers with experience.13,27Angiography provides the best characterization of theextent of chronic thromboembolic disease and the deter-mination if the disease is present in surgically approach-able vessels The angiographic appearance of chronicthromboemboli differs from acute pulmonary embolus.Rather than the well-delineated intraluminal fillingdefects seen in acute pulmonary emboli, patients withCTPH have defects that are irregular and partiallyrecanalized and which may appear as bands or webs.Angioscopy employing a fiberoptic device has also beenused to characterize CTPH patients However, this is notwidely available

Angioscopy has been used at its originating center tohelp characterize the extent of thromboembolism inpatients with milder pulmonary hypertension and ques-

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tionable angiographic findings and to determine

operabil-ity in patients with severe pulmonary hypertension with

inadequate findings on angiography to justify surgery.28

Pulmonar y thromboendarterectomy remains a

complicated procedure that is best carried out at centers

with expertise In the most experienced hands, the

mortality is 7%, with reports of mortality ranging as high

as 24%.10Reperfusion injury following the procedure

remains the major cause of morbidity and mortality The

surgery is contraindicated in patients with severe

under-lying lung disease Advanced age, severe right heart

fail-ure, and significant collateral disease are relative

contraindications Coronary artery angiography is

performed for all patients with risk factors for coronary

artery disease with the possibility of coronary artery

bypass grafting concurrent with

thromboendarterec-tomy, if warranted Placement of an inferior venacaval

filter is recommended prior to surgery to assure that

pulmonary embolism does not recur Following the

thromboendarterectomy, a reduction in the pulmonary

vascular resistance of approximately 65% is expected

This is associated with improvements in gas exchange

and exercise tolerance with patients improving from New

York Heart Association class III or IV to class I or II after

surgery Lifelong anticoagulation is recommended

A subgroup of patients who have had acute

pul-monary embolism with apparent resolution or who have

chronic thromboembolic disease in the pulmonary artery

but of an extent too small to explain the progression and

severity of pulmonary hypertension present with a

syndrome very similar to PPH Once these patients are

ruled out as candidates for surgical therapy, the medical

therapies recommended for PPH are appropriate An

inferior venacaval filter should be considered if there is

any question of failure of anticoagulation therapy

Pulmonary Veno-Occlusive Disease

Pulmonary veno-occlusive disease (PVOD) was initially

recognized as a subcategory of PPH The presentation of

PVOD is clinically similar to PAH.29However, a

patholog-ical hallmark is the diffuse occlusion of pulmonary veins

by fibrous tissues Pathological findings suggest evolution

of the fibrotic lesions from loose, edematous fibrosis to

dense, sclerotic fibrosis Typically, intimal involvement is

seen in venules and smaller veins, but involvement of

larger veins can be seen as well Medial thickening tends

to be eccentric and heterogenous as seen in the small

arterioles in PAH In time the thickened intima may

become arterialized and completely occluded vessels may

become revascularized.30

It is felt that the cause of elevated pulmonary vascular

resistance lies in the venous changes As might be

ex-pected in response to the raised pulmonary artery sures, the pulmonary arterioles may demonstrate medialhypertrophy, but other findings of pulmonary arterialhypertension such as plexiform lesions are absent.PVOD, historically, accounted for 5 to 25% of PAH Asfor PAH, the age of onset spans life expectancy.2 9However, unlike for PAH, the ratio of men to women isapproximately 1:1 Infections with various agents havebeen suggested as leading to PVOD Some of these agents

pres-are Toxoplasma gondii, measles, Epstein-Barr virus,

cytomegalovirus, and HIV A genetic risk has beensuggested by case reports in siblings, but unlike PPH, nogene has, as yet, been linked to the condition A casereport suggested an association with sniffing cleaningpowder.31A better-characterized association has beenfound with chemotherapy including bleomycin, mito-mycin, and carmustine and with both allogeneic andautologous bone marrow transplantation.32,33An autoim-mune association has been suggested by the presentation

of patients with associated myopathy, alopecia, toid arthritis, systemic lupus erythematosus, CRESTsyndrome, and positive antinuclear antibodies However,these associations are missing in most individuals

rheuma-A distinguishing radiographic feature of PVOD is thepresence of radiographic changes in the pulmonaryparenchyma.34Since the vascular obstruction is postcapil-lary, the pulmonary capillaries are exposed to higherpressures and, thus, radiographic changes associated withinterstitial edema may be observed, such as Kerley’s Blines and pleural effusions Patchy pulmonary infiltratesmay be observed as well and, when present, may be asso-ciated with crackles on physical exam On high-resolution CT scan, ground glass opacities, thickenedseptal lines, and multiple small nodules have beenobserved

Physiologically, there is little to distinguish PVODfrom PAH Cardiac catheterization will show elevatedpulmonary artery pressures and, if the pulmonary arterycatheter is successfully wedged, normal pulmonary arterywedge pressures Failure to obtain a pulmonary arterywedge pressure tracing is common in PVOD.34In thepulmonary function lab, the diffusion capacity of thelung for carbon monoxide is usually reduced Spirometryand lung volumes may be normal or demonstrate arestrictive impairment

The finding of PAH, evidence of pulmonary edema onthe chest radiograph, and normal ventricular functionhas been suggested to be diagnostic of PVOD However,patients with PVOD may not demonstrate radiologicalfindings Open lung biopsy is a possible approach for thedefinitive diagnosis of PVOD Confirming the diagnosishas been felt to be appropriate as treatment withvasodilators may be hazardous An alternative approach

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is to cautiously test the hemodynamic response of

patients with suspected PVOD with short-acting

vasodilators during cardiac catheterization prior to

initi-ation of therapy

Patients with PVOD are at increased risk for the

administration of pulmonary vasodilators.35,36The

dila-tion of pulmonary arterioles, in the presence of fixed

venous occlusion, can lead to sudden increase in

pulmonar y capillar y pressure with formation of

pulmonary edema and even death However, as PVOD is

a relentlessly progressive and fatal disease, cautious

administration of vasodilators may be warranted The

response of PVOD to vasodilators is not well established

However, some studies have suggested alleviation of

elevated pulmonary vascular resistance in response to

vasodilators.37Similarly, anticoagulation is suggested

based on the experience with PPH Oxygen should be

administered to hypoxic patients If therapeutic

modali-ties fail, then PVOD becomes an indication for

consider-ation for lung transplantconsider-ation

Pulmonary hypertension may also result from the

occlusion of large pulmonary veins Inflammatory

diseases or neoplastic diseases of the mediastinum can

impinge upon and obstruct the pulmonary veins

Fibro-sing mediastinitis is a rare cause of pulmonary vein

occlusion It is characterized by exuberant fibrotic

re-sponse to inflammation in mediastinal lymph nodes,

which often spills over into other mediastinal structures

Some cases have been associated with histoplasmosis

infections by the finding of organisms on culture of

surgical specimens, while other cases have no clear

docu-mented etiology Successful surgical bypass of the

affected veins has been reported Case reports suggest

efficacy for treatment with tamoxifen

Lung Disease Associated with

Pulmonary Hypertension

Secondary causes of pulmonary hypertension are by far

more common than PAH, and the most common cause

of secondary pulmonary hypertension is lung diseases

The initial presentation of pulmonary hypertension

asso-ciated with lung diseases is that of the underlying lung

disease Lung diseases commonly associated with

pulmonary hypertension include COPD, restrictive lung

disease including the interstitial lung diseases, and

syndromes associated with hypoventilation

A central characteristic of these diseases is alveolar

hypoxia Alveolar hypoxia causes vasoconstriction

Teleologically, this mechanism helps to recruit

pulmonary vascular circulation distant from an area of

injury (eg, an underventilated portion of the lung

involved with pneumonia) When the alveolar hypoxia

becomes global, the vasoconstriction results inpulmonary hypertension Persistent alveolar hypoxialeads to vascular smooth muscle hypertrophy and vascu-lar remodeling eventually leading to fixed pulmonaryhypertension.38

Other mechanisms unique to the underlyingpulmonary pathology are associated with pulmonaryhypertension caused by pulmonary diseases In COPD,emphysematous changes lead to loss of alveolar septa andthe associated pulmonary capillary bed Progressive airtrapping leads to raised intra-alveolar pressure, which hasthe effect of collapsing alveolar vessels, further contribut-ing to the raised pulmonary artery pressure In COPD,factors that exacerbate hypoxia such as desaturation withexercise or desaturation associated with sleep-disorderbreathing can worsen the pulmonary hypertension.39The therapeutic approach to pulmonary hypertension

in COPD is to maximize bronchodilation, relieving areas

of poor ventilation and air trapping, and supplementaloxygen, especially during periods of increased physiolog-ical stress such as with exercise and sleep.40

Pulmonary hypertension associated with COPD tends

to occur in more severe lung disease and is predictive ofmortality.41However, the correlation between pulmonaryfunction tests and pulmonary hypertension in COPD issomewhat variable Patients who have a predominantlychronic bronchitic picture, with severe ventilation–perfusion mismatch and sleep-disorder breathing, canhave pulmonary hypertension fairly early in the course oftheir disease On the other hand, patients with a primar-ily emphysematous picture do not tend to developpulmonary hypertension until the forced expiratoryvolume in 1 second drops well below 1 L The best deter-minants for suspicion of pulmonary hypertension inpatients with COPD are the clinical findings of corpulmonale.42, 43

Restrictive lung diseases can be associated withpulmonary hypertension as well Restrictive lung diseasesare defined by impairment of the total lung capacity.These can be divided into a group of diseases that causeparenchymal lung disease and those that cause abnor-malities of the muscles of respiration and the thoraciccage The former group includes idiopathic interstitiallung diseases (eg idiopathic pulmonar y fibrosis,eosinophil granuloma, and sarcoidosis) and the pneumo-conioses (eg, asbestosis and hypersensitivity pneumoni-tis) The latter group includes diseases causing grossdistortions of the thoracic cage such as severe kyphoscol-iosis and neuromuscular disorders, which affect thediaphragm

The fibrosing interstitial lung diseases cause monary hypertension in part through the mechanismsassociated with alveolar hypoxia Additionally, progres-

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pul-sive fibrosis causes destruction of normal parenchymal

structures leading to distortion and destruction of the

pulmonary vasculature.44Pulmonary hypertension can

occur with exercise in patients with fairly well-preserved

lung volumes (total lung capacity in the range of 50 to

80% of predicted) Pulmonary hypertension at rest tends

to occur when total lung capacity falls below 50%

The treatment of interstitial lung diseases, once

fibro-sis has occurred, is universally disappointing Specific

therapies for some conditions such as prednisone for

sarcoidosis and prednisone and removal from exposure

to the inciting agent in hypersensitivity pneumonitis can

be quite effective early in the course of the disease at a

stage in the disease preceding the usual appearance of

pulmonary hypertension

Recently, an association has been described between

pulmonary hypertension and sarcoidosis In a subset of

patients with sarcoidosis, pulmonary artery pressures have

been known to be elevated and progressive in a manner

similar to that in PAH These patients are now classified as

a subgroup of patients with conditions that directly affect

the pulmonary vessels Patients with sarcoidosis and

pulmonary hypertension should be evaluated and treated

medically as described above for patients with PAH.45

Disorders of the muscles of respiration and the

thora-cic cage cause pulmonary hypertension through a variety

of mechanisms.46 The most obvious is hypoxia due to

hypoventilation However, the distribution of ventilation

is not homogenous, leading to areas of atelectasis and of

exaggerated ventilation–perfusion mismatch, which

contribute to alveolar hypoxia, vasoconstriction, and

even-tual fixed vascular changes of pulmonary hypertension

The treatment of pulmonary hypertension for

pa-tients with disorders of ventilation is primarily

mechani-cal in nature Supplemental oxygen can minimize the

severity and progression of pulmonary hypertension

However, the atelectasis and uneven distribution of

ventilation can only be addressed by mechanical support

Nocturnally administered continuous positive airway

pressure or bilevel positive airway pressure (BiPAP) can

be efficacious However, if the condition results from a

progressive disease, such as multiple sclerosis, then full

mechanical support via tracheostomy may be indicated

Treatment of pulmonary hypertension associated with

pulmonary diseases by the use of vasodilators has not

been shown to be effective Anecdotal reports have

suggested efficacious response in individuals, but control

trials have not supported vasodilator therapy

Theoretically, vasodilation of diseased lungs would be

expected to cause a variable response across the vascular

bed possibly leading to worsening of ventilation–

perfusion mismatch and, in turn, more severe alveolar

do the pulmonary venous pressures; vascular remodelingoccurs on the arterial side in response to chronic increase

in a passively increased pulmonary artery pressure.PAH can also be a manifestation of high flow states.48Congenital abnormalities of the heart, such as ventricularseptal defect, atrial septal defect, and patent ductus arterio-sus, are associated with left-to-right shunts Chronic expo-sure of the pulmonary arterial bed to high flow leads toinitially reversible changes of medical hypertrophy and inti-mal hyperplasia but eventually will be characterized byocclusion of vascular lumens by intimal hyperplasia andthe formation of plexiform lesions Repair of the congenitalanomaly while the lesions are still reversible can potentiallylead to normalization of the pulmonary artery pressure.Echocardiography with infusion of saline bubbles is effec-tive for demonstrating shunts Transesophageal echocardio-graphy is especially useful for the investigation of theintra-atrial septa Sampling of the oxygen content of theblood at the time of right heart catheterization can alsodocument a left-to-right shunt Finally, measurement of thepulmonary artery wedge pressure will confirm the diagno-sis of left ventricular dysfunction

Surgical Implications of Pulmonary

Trang 18

occur, if possible, prior to surgery Vasodilator therapy

should be optimized and clinical conditions contributing

to secondary pulmonary hypertension, such as hypoxia,

should be corrected when possible.50In cases of acute PAH

due to pulmonary embolism, acute interventions with

more selective pulmonary vasodilators, such as inhaled

nitric oxide or epoprostenol infused into the central

venous system, may assist in control of hemodynamic

status Pulmonary hypertension is an indication for

intra-operative monitoring with a pulmonary artery catheter to

provide for more precise control of volume status Patients

with PAH anticoagulated with warfarin should not have

their anticoagulation discontinued, if possible, until the

time of surgery Either the anticoagulation can be reversed

and the patient placed on heparin, or the warfarin may be

discontinued and bridged to operation using daily

injec-tions of low molecular weight heparin

References

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2 Rich S, Dantzker DR, Ayres SM, et al Primary pulmonary

hypertension A national prospective study Ann Intern

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3 McQuillan BM, Picard MH, Leavitt M, Weyman AE.

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normal subjects Circulation 2001;104:2797–802.

4 Rubin LJC Primary Pulmonary Hypertension; ACCP

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5 Rubin LJ Primary pulmonary hypertension N Engl J Med

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7 Archer S, Rich S Primary pulmonary hypertension A

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progress” Circulation 2000;102:2781–91.

8 Newman JH, Wheeler L, Lane KB, et al Mutation in the

gene for bone morphogenetic protein receptor II as a cause

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9 Loscalzo J Genetic clues to the cause of primar y

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10 Fedullo PF, Auger WR, Kerr KM, Rubin LJ Chronic

throm-boembolic pulmonar y hypertension N Engl J Med

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11 Abenhaim L, Moride Y, Brenot F, et al Appetite-suppressant

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Group N Engl J Med 1996;335:609–16.

12 Rich S, Pietra GG, Kieras K, et al Primary pulmonary hypertension: radiographic and scintigraphic patterns of histologic subtypes Ann Intern Med 1986;105:499–502.

13 Nicod P, Peterson K, Levine M, et al Pulmonary phy in severe chronic pulmonary hypertension Ann Intern Med 1987;107:565–8.

angiogra-14 Kessler R, Chaouat A, Weitzenblum E, et al Pulmonary hypertension in the obstructive sleep apnoea syndrome: prevalence, causes and therapeutic consequences Eur Respir J 1996;9:787–94.

15 Rich S, Kaufmann E High dose titration of calcium nel blocking agents for primary pulmonary hypertension: guidelines for short-term drug testing J Am Coll Cardiol 1991;18:1323–7.

chan-16 Rich S, Kaufmann E, Levy PS The effect of high doses of calcium-channel blockers on sur vival in primar y pulmonary hypertension N Engl J Med 1992;327:76–81.

17 McLaughlin VV, Genthner DE, Panella MM, Rich S Reduction in pulmonary vascular resistance with long-term epoprostenol (prostacyclin) therapy in primary pulmonary hypertension N Engl J Med 1998;338:273–7.

18 Rubin LJ, Badesch DB, Barst R, et al Bosentan therapy for pulmonar y arterial hy pertension N Engl J Med 2002;346:896–903.

19 D’Alonzo GE, Barst RJ, Ayres SM, et al Survival in patients with primary pulmonary hypertension Results from a national prospective registr y Ann Intern Med 1991;115:343–9.

20 Conte JV, Gaine SP, Orens JB, et al The influence of uous intravenous prostacyclin therapy for primar y pulmonary hypertension on the timing and outcome of transplantation J Heart Lung Transplant 1998;17:679–85.

contin-21 Moser KM, Bloor CM Pulmonary vascular lesions ring in patients with chronic major vessel thromboembolic pulmonary hypertension Chest 1993;103:685–92.

occur-22 Jamieson SW, Kapelanski DP Pulmonary endarterectomy Curr Probl Surg 2000;37:165–252.

23 Auger WR, Moser KM Pulmonary flow murmurs: a distinctive physical sign found in chronic pulmonary thromboembolic disease Clin Res 1989;37:145A.

24 Wolf M, Boyer-Neumann C, Parent F, et al Thrombotic risk factors in pulmonary hypertension Eur Respir J 2000;15:395–9.

25 Auger WR, Permpikul P, Moser KM Lupus anticoagulant, heparin use, and thrombocytopenia in patients with chronic thromboembolic pulmonary hypertension: a preliminary report Am J Med 1995;99:392–6.

26 Fishman AJ, Moser KM, Fedullo PE Perfusion lung scans vs pulmonary angiography in evaluation of suspected primary pulmonary hypertension Chest 1983;84:679–83.

27 Pitton MB, Duber C, Mayer E, Thelen M Hemodynamic effects of nonionic contrast bolus injection and oxygen inhalation during pulmonary angiography in patients with chronic major-vessel thromboembolic pulmonary hyper- tension Circulation 1996;94:2485–91.

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28 Sompradeekul S, Fedullo PF, Kerr KM, et al The role of

pulmonary angioscopy in the preoperative assessment of

patients with thromboembolic pulmonary hypertension

(CTEPH) Am J Respir Crit Care Med 1999;159:A456.

29 Mandel J, Mark EJ, Hales CA Pulmonary veno-occlusive

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primary pulmonary hypertension: a qualitative and

quanti-tative study of pulmonary blood vessels from 58 patients in

the National Heart, Lung, and Blood Institute, Primary

Pulmonar y Hy pertension Registr y Circulation

1989;80:1198–206.

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disease: etiological and therapeutic appraisal Angiology

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chemotherapy and hormonotherapy Curr Opin Oncol

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Malignancy-associated pulmonary veno-occlusive disease: report of a

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of the chest in four patients with pulmonary capillary

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J Roentgenol 1998;171:1321–4.

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with pulmonar y veno-occlusive disease Chest

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37 Davis LL, deBoisblanc BP, Glynn CE, et al Effect of

prosta-cyclin on microvascular pressures in a patient with

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38 Cutaia M, Rounds S Hypoxic pulmonary vasoconstriction:

physiologic significance, mechanism, and clinical relevance.

Chest 1990;97:706–18.

39 Douglas NJ, Flenley DC Breathing during sleep in patients with obstructive lung disease Am Rev Respir Dis 1990;141(4 Pt 1):1055–70.

40 Salvaterra CG, Rubin LJ Investigation and management of pulmonary hypertension in chronic obstructive pulmonary disease Am Rev Respir Dis 1993;148:1414–7.

41 Bishop JM, Cross KW Physiological variables and mortality

in patients with various categories of chronic respiratory disease Bull Eur Physiopathol Respir 1984;20:495–500.

42 Oswald-Mammosser M, Apprill M, Bachez P, et al Pulmonar y hemodynamics in chronic obstructive pulmonary disease of the emphysematous type Respiration 1991;58:304–10.

43 Traver GA, Cline MG, Burrows B Predictors of mortality in chronic obstructive pulmonary disease: a 15-year follow-up study Am Rev Respir Dis 1979;119:895–902.

44 Enson Y, Thomas HM, Bosken CH Pulmonary sion in interstitial lung disease: relation of vascular resis- tance to abnormal lung structure Trans Assoc Am Physicians 1975;88:248–55.

hyperten-45 Preston IR, Klinger JR, Landzberg MJ, et al Vasoresponsiveness of sarcoidosis-associated pulmonary hypertension Chest 2001;120:866–72.

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47 Dexter L Pulmonary vascular disease in acquired heart disease In: Moser KM, editor Pulmonary vascular disease New York: Marcel Dekker; 1979 p 427–88.

48 Rabinovitch M Mechanisms of pulmonary hypertension in chronic high flow states In: Weir EK, Reeves JT, editors Pulmonary vascular physiology and pathophysiology New York: Marcel Dekker; 1989 p 469–512.

49 Hohn L, Schweizer A, Morel DR, et al Circulatory failure after anesthesia induction in a patient with severe primary pulmonary hypertension Anesthesiology 1999;91:1943–5.

50 Kaplan J, Reich D, Konstadt S, Stammers A Cardiac thesia 1999.

Trang 20

Pulmonar y hy pertension as a result of chronic

pulmonary thromboembolic disease is a common yet

underdiagnosed condition Patients with this syndrome

may present with a wide variety of debilitating

pulmonary or cardiac symptoms Once properly

diag-nosed, the only curative treatment is surgical removal of

the disease, by means of pulmonary

thromboendarterec-tomy (PTE) Medical management is only palliative, and

surgery by means of transplantation is an inappropriate

use of resources with less than satisfactory results

PTE is a technically demanding yet highly successful

operation for chronic pulmonary thromboembolic

disease The procedure is widely misunderstood, and

though many have attempted it, it is performed with

success at only a few centers Proper patient selection,

meticulous surgical technique, and careful postoperative

management at selected centers have now clearly shown

that it is an effective therapy The operation seems

diffi-cult to perform well; a true endarterectomy (not an

embolectomy) of all affected parts of the lung remains the

key to success This chapter considers the place of the

operation in the spectrum of patients with pulmonary

hypertension and describes the preoperative work-up, the

technical details of the operation, and the current results

at the University of California, San Diego (UCSD)

Pulmonary hypertension is a manifestation of manycardiac and pulmonary diseases Cardiac causes includethe result of congenital and acquired heart disease Thepulmonary causes can be divided in three general cate-gories: primary, parenchymal, and vascular In primarypulmonar y hypertension, the microvasculature isaffected by an uncertain process, which is generallyconsidered progressive and irreversible Parenchymalpulmonary disease includes a group of patients with anunderlying pulmonary disease, such as emphysema orpulmonary fibrosis, which could progress in pulmonaryhypertension Pulmonary vascular causes refer topatients with acute and chronic pulmonary thromboem-bolic disease, as well as pulmonary veno-occlusivedisease

The prognosis for patients with pulmonary sion is poor, and it is worse for those who do not haveintracardiac shunts Thus, patients with primar ypulmonary hypertension and those with pulmonaryhypertension due to pulmonary emboli fall into a higherrisk category than those with Eisenmenger’s syndromeand encounter a higher mortality rate In fact, once themean pulmonary pressure in patients with thromboem-bolic disease reaches 50 mm Hg or more, the 3-yearmortality approaches 90%.1

Trang 21

hyperten-Patients with pulmonary hypertension present one of

the more difficult therapeutic challenges Medical

treat-ment is generally unsatisfactory and palliative at best

Surgical options are dependent on both the primary

disease process and the reversibility of the pulmonary

hypertension With the exception of thromboembolic

pulmonary hypertension, lung transplantation is the only

effective therapy for patients with pulmonary

hyperten-sion, when the disease reaches end-stage Pulmonary

transplantation is also still used in some centers as the

treatment of choice for those with thromboembolic

disease However, a true assessment of the effectiveness of

any therapy should take into account the total mortality

once the patient has been accepted and put on the

wait-ing list Thus, the mortality for transplantation (and

especially double-lung transplantation) as a therapeutic

strategy is much higher than is generally appreciated

because of the significant loss of patients awaiting

donors In addition, the long-term use of anti-rejection

medications with their associated side effects, the higher

operative morbidity and mortality, and the long waiting

time clearly make transplantation an inferior option to

PTE, and we consider it to be inappropriate

PTE should be applied as a treatment for

thromboem-bolic disease whenever possible, provided acceptable

results can be achieved It reduces the mortality rate of

patients on the waiting list and avoids

immunosuppres-sion Further, it appears to be permanently curative

Embolic Pulmonary Hypertension

Laennec originally described pulmonary embolism in

1819, and related the condition to deep venous

thrombo-sis.2Virchow recognized that the three factors

predispos-ing to venous thrombosis were stasis, hypercoagulability,

and vessel wall injury.3Despite our progressive

under-standing of the etiology and pathology of this condition,

deep venous thrombosis with subsequent pulmonary

thromboembolism remains a significant cause of

morbidity and mortality Acute pulmonary embolism,

after cancer and heart disease, remains the third most

common cause of death in the United States

Acute pulmonary thromboembolism is thus a much

more common condition than is generally appreciated,

and in many cases, it is asymptomatic Dalen and Alpert

in 1975, calculated that pulmonary embolism resulted in

630,000 symptomatic episodes in the United States

yearly, making it, at the time, about one-half as common

as acute myocardial infarction and three times as

common as cerebral vascular accidents.1However, this

may be a low estimate, since autopsy studies have shown

that the diagnosis of acute pulmonary embolism was

unsuspected in 70 to 80% of those patients in whom it

was the principal cause of death.4,5Another autopsyanalysis of 13,216 patients showed pulmonary throm-boembolism in 5.5%, and up to 31.3% in the elderly.6

It is almost axiomatic that heightened interest in a given disease leads to an increased incidence of discovery Therefore current opinions regarding the rarity of exten- sive pulmonary thromboembolism may well be revised in the future, and available estimates of its incidence should

be viewed in this light 7

In addition to patients suffering from acutepulmonary embolism from deep vein thrombosis, thereare other special circumstances For example chronicindwelling central venous catheters and pacemaker leadscan be associated with pulmonary emboli Patients withintracardiac shunts who develop pulmonary hyperten-sion may have other factors involved, such as directchemical irritation of the pulmonary vascular bed Otherrare causes include tumor emboli; tumor fragments fromkidneys, breasts, and stomach have been demonstrated tocause chronic pulmonary arterial occlusion Tumoremboli could also originate from right atrial myxomas.However, not every case is the result of embolic material

In situ thrombosis, either as a result of coagulopathy,endothelial damage, or a secondary phenomenon after aninitial embolism has well been described

What happens to the embolic material, once wedged

in the pulmonary artery, depends on a few differentfactors In the majority of patients, spontaneous resolu-tion of acute pulmonary emboli is the rule However, asmall but uncertain percentage develop chronic throm-boembolic pulmonary hypertension Again, the mecha-nisms responsible for the failure of the body to dissolvethe material remain unclear The volume of the embolicmaterial may simply be too overwhelming for the lyticmechanisms The emboli may be made of a substancethat cannot be resolved—materials such as already well-organized fibrous thrombus, fat, or tumor Further,repetitive emboli may not be able to be resolved On theother hand, there may be an abnormal lytic mechanism,

or some patients may have a propensity for thrombus or

Trang 22

arteries in nearly 1% of 7,753 autopsies.8This remains a

low estimate for the incidence of operable pulmonary

hypertension, since many patients who have had relief of

their pulmonary hypertension following PTE have had

disease confined to their minor pulmonary arteries, and

chronic thrombus in these smaller pulmonary vessels is

probably often overlooked in autopsy series

The vast majority of cases of pulmonary hypertension

due to pulmonary artery occlusion are the result of

“spontaneous” thromboembolism In a small percentage

(5 to 11%), however, coagulation abnormalities can be

detected, such as lupus anticoagulant, protein C

defi-ciency, or antithrombin III deficiency.9A few patients

have a paradoxical response to heparin, with apparent

heparin-induced platelet antibodies In such cases,

special precautions must be taken during

cardiopul-monary bypass and the perioperative period, and great

care must be taken to eliminate heparin from all

intra-venous lines Studies of the pulmonary vascular

endothe-lium in affected patients have failed to demonstrate any

consistent abnormality; however, an elevation in factor

VIII-related antigen has been shown to occur in

associa-tion with extensive intimal damage.10,11

After a pulmonary embolus, the unresolved residual

pulmonary artery clot organizes and obstructs the

pulmonary arteries to a variable extent, at the main

pulmonary artery, lobar, segmental, or subsegmental

level.8The resultant pulmonary vascular hypertension

may be a very complex process, and factors other than

the simple hemodynamic consequences of redirected

blood flow with higher pressures and flow are most likely

involved In general, more than 50% of the pulmonary

vasculature must be occluded for patients to become

pulmonary hypertensive However, very frequently we

encounter patients with significant pulmonary

hyperten-sion with less than 50% of the vascular bed occluded by

thromboembolic material There may be a sympathetic

neural, hormonal, or combined neurohormonal signal

that initiates pulmonary hypertensive changes on the

initially unaffected pulmonary vascular bed—a process

that can occur in either lung, regardless of the original

site of occlusion In these cases, the operation will open

the vessels occluded by the thromboembolic material or

intimal hyperplasia but cannot resolve the small-vessel

disease of reactive pulmonary hypertension (Figures

24-1–24-3)

Irrespective of the exact etiology, the resultant

pulmonary hypertension and the secondary vasculopathy

is a serious debilitating condition, potentially inoperable

With our increasing experience with patients with

thromboembolic pulmonary hypertension, we have

become much more inclined toward early operation to

avoid these deleterious consequences

FIGURE 24-1 A, Pulmonary artery (PA) chest film of a 72-year-old

physician with severe pulmonary hypertension (PA pressure above systemic levels, pulmonary vascular resistance 1,250 dynes/sec/cm 5 ) Note the right heart enlargement, prominent pulmonary artery shadow,

and hypoperfusion of areas of right and left lungs B, Lateral view of

chest Note right heart enlargement and anterior proximity to sternum.

Trang 23

thrombosis should be sought, as should a history of leg

swelling, chest pain, cough, hemoptysis, or anything to

indicate episodes of pulmonary embolism The initial

symptoms, being vague, are often attributed to other

causes, such as coronary or myocardial disease,

intersti-tial lung disease, asthma, or age Many cases remain

undiagnosed, especially since the patients may be

asymp-tomatic and have normal pulmonary artery pressures at

rest Other symptoms that may occur, usually in the later

stages of the disease, include exertional chest pain, cough,

and hemoptysis

Physical Examination

Clinical examination is usually nonproductive and

unre-warding if right heart failure has not developed, even if the

patient has a history of severe dyspnea Cyanosis is usually

absent, unless it is peripheral and related to severely

depressed cardiac output or central as the result of

right-to-left shunting in the setting of patent foramen ovale or

an atrial septal defect Clubbing of the fingers is not

usually present Flow murmurs may be heard, especially

over the back, owing either to flow through narrowed

pulmonary arteries or to aggressive bronchial flow

Diagnostic Tests

Chest roentgenogram, electrocardiogram, and pulmonary

function tests are of little value in differentiating

throm-boembolic pulmonary hypertension from other forms of

pulmonary hypertension However, these investigations

often give the initial clues that pulmonary hypertension

exists when the physical findings are less conclusive

The radiographic signs of pulmonary hypertension on

chest film may be difficult to determine Enlargement of

the pulmonar y arter y and paucity of flow to the

pulmonary vascular bed may indicate occlusion of major

vessels (see Figure 24-1A) The lateral chest film will often

show right ventricular hypertrophy (see Figure 24-1B)

Echocardiography demonstrates enlarged right-sided

heart chambers and varying degrees of tricuspid

regurgi-tation Standard two-dimensional echocardiography is

also helpful in defining the presence and severity of

pulmonary hypertension and excluding certain other

causes such as Eisenmenger’s syndrome

Continuous-wave Doppler echocardiography of the tricuspid

regurgi-tant jet will estimate the pulmonary artery systolic

pressure Occasionally, proximal, chronic, organized

thrombus in the main pulmonary artery or main right

and left pulmonary arteries can be seen with transthoracic

echocardiography; however, this technique lacks

sensitiv-ity and is inadequate for visualization of the lobar vessels,

where the embolic material is often localized

Transesophageal echocardiography has proved to be more

promising, especially with multiplane probes that allow

angulation of the imaging plane so that the origin of most

of the lobar vessels can be identified Early attempts arebeing carried out at visualizing the pulmonary arterieswith transbronchial echocardiography

A perfusion scan is almost always performed Themajor differential diagnosis is primary pulmonary hyper-tension, in which the scan is usually normal or has apatchy and mottled appearance, in contrast to the multi-ple punched-out lobar or segmented defects of chronicthromboembolic disease The perfusion scan tends tounderestimate the degree of occlusion of the pulmonaryvessels A computed tomography (CT) scan may beuseful,12 and recent work has been performed usingcomputer-enhanced images of CT scanning, both in theacute and chronic forms of this condition These imagesare capable of confirming occlusion in at least the mainand lobar pulmonary arteries Further, a mosaic pattern

of lung attenuation on CT is a sign of variable regionalperfusion and may suggest chronic pulmonary throm-boembolism as a cause for pulmonary hypertension.13Once pulmonary hypertension as a result of chronicthromboembolic disease is suspected, the evaluation ofthe patient prior to planning surgical interventiondepends on right heart catheterization and pulmonaryangiography These are essential to evaluate the severity

of pulmonary hypertension, to define the presence ofthromboembolic disease, to assess the operative risk andsurgical accessibility, and to exclude other diagnoses Insome patients with only moderate pulmonary hyperten-sion at rest, a striking increase in pulmonary artery pres-sure will be seen with only minimal exercise Thoughconcern is regularly expressed that angiography placesthe pulmonary hypertensive patient at great risk, we havenot found this to be the case,14and pulmonary arteriog-raphy is performed on pulmonary hypertensive patients

on almost a daily basis at our center

Selective power injections of the right and leftpulmonary trunks, using nonionic contrast agents toprevent the cough response, are well tolerated The typi-cal findings of chronic thromboembolic disease onpulmonary angiogram include an irregular lumen, indi-cating thrombus attached to the vessel wall, and theappearance of bands or webs across the lumen of vessels,sometimes with poststenotic dilatation Other findingsmay include occlusion of branches with lack of filling out

to the periphery, often with an abrupt termination ofpulmonary vessels with a pouch-like appearance (Figures24-2 and 24-4)

In addition to pulmonary angiography, patients over

35 years of age undergo coronary arteriography andother cardiac investigation as necessary If significantdisease is found, additional cardiac surgery is performed

at the time of PTE

Trang 24

Most patients referred for PTE surger y have a

pulmonary vascular resistance of more than 1,000

dynes/sec/cm 5, and many have suprasystemic

pulmonary artery pressures We have operated on

patients ranging in age from 14 to 83 years The

docu-mented history of pulmonary vascular occlusion has

been as brief as a few months to as long as 24 years Prior

to PTE surgery, an inferior vena cava filter is always

placed Patients are thereafter treated with anticoagulants

indefinitely

Operation

There are some guiding principles that are essential to a

successful outcome in this challenging operation First,

the operation must be performed on both lungs, since

patients with significant chronic embolic pulmonary

hypertension invariably have bilateral disease Second,

cardiopulmonary bypass (CPB), with periods of

circula-tory arrest, is essential to achieve adequate exposure in

the face of the copious bronchial blood flow Third, a

true endarterectomy in the plane of the media must be

accomplished

It is essential to appreciate that the removal of visible

thrombus is largely incidental to this operation Indeed,

in the majority of patients, no free thrombus is present,

and on initial direct examination the pulmonary vascular

bed may appear normal

The operation is thus performed through a median

sternotomy and on cardiopulmonary bypass.20 This

allows a bilateral approach and also the use of circulatory

arrest under profound hypothermia The circulatory

arrest periods are limited to 20 minutes, with restoration

of flow between each interruption With our increased

experience, the endarterectomy usually can be performed

with a single period of circulatory arrest on each side

Although retrograde cerebral perfusion has been

advo-cated for total circulatory arrest in other procedures, it is

not helpful in this operation since it does not allow a

completely bloodless field, and with the short arrest

times that can be achieved with experience, it is not

necessary During circulatory arrest, progressive

circum-ferential dissection is carried into all the involved lobar,

segmental, and subsegmental vessels With proper

expo-sure, all the residua of thromboembolic occlusion can be

removed, no matter how distal, and it is possible to

remove occluding material as far distally as the

diaphrag-matic level

The patient is prepared as for any open-heart

proce-dure, with arterial and pulmonary artery catheters and

electroencephalogram monitoring A femoral artery line

is also placed because the profound vasoconstriction that

tends to occur after hypothermic circulatory arrest makes

readings from the radial artery catheter unreliable duringthe immediate postoperative period A median ster-notomy incision is made and the sternum divided Theright heart is invariably enlarged, with variable degrees oftricuspid regurgitation

Bypass is instituted with high ascending aortic lation and two caval cannulae Standard flow forcardiopulmonary perfusion is used and the patientcooled, maintaining a 10°C gradient between arterialblood and bladder or rectal temperature.21

cannu-A temporarypulmonary artery vent is inserted Once ventricularfibrillation occurs, a second vent is placed in the leftatrium through the right upper pulmonary vein Thisprevents distention from the large amount of bronchialarterial blood flow that is common with these patients.The patient’s head is surrounded by ice and the cool-ing blanket turned on During perfusion the venous satu-rations increase; saturations of 80% at 25°C and 90% at20°C are typical Hemodilution is carried out to decreasethe blood viscosity during hypothermia and to optimizecapillary blood flow The hematocrit is maintained in therange of 18 to 25 during profound hypothermia.Phenytoin is administered intravenously during cooling

at 15 mg/kg, to a maximum dose of 1 g

During the cooling period some preliminary tion can be carried out, with full mobilization of theascending aorta from the pulmonary artery The superiorvena cava is mobilized all the way to the innominate veinand dissected free of the right pulmonary artery Theazygos vein is exposed but not divided The reflection ofthe right pulmonary artery to the left atrium is separated.Most of this dissection is performed with electrocautery,because with advanced right heart failure and hepaticcongestion, coagulation is usually abnormal However,care must be taken to preserve the integrity of the rightphrenic nerve lying lateral to the superior vena cava Alldissection of the pulmonary arteries occurs intrapericar-dially, and it is not necessary to enter either pleuralcavity

dissec-The right pulmonary artery is now exposed so that thetake-off of upper and middle lobes can be seen Theupper pulmonary vein is usually not visualized butreflected upward from the plane of the pulmonary arterywall An incision is made in the right pulmonary arteryfrom beneath the ascending aorta out under the superiorvena cava and entering the lower lobe branch of thepulmonary artery just after the take-off of the middlelobe It is important that the incision stay in the center ofthe vessel Only one incision is needed, and it is easier toendarterectomize the right upper lobe from a centralincision than through a separate incision in the upperlobe artery The distal limit of the incision is usuallyapproximately 1 cm distal to the take-off of the upper

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