Studies on the Structure of the Pulmonary Trunk I. Normal Changes in the Elastic Configuration of the Human Pulmonary Trunk at Different Ages By MARIO SALDANRA, M.D., AND JAVIER ARIAS-STELLA, M.D. IN AN EARLIER study, Heath, Wood, DuShane, and Edwards' have pointed out the morphologic characteristics of the elastic tissue in the trunk of the pulmonary artery in cases of congenital and acquired cardiopa- thies. Among 71 "control" cases that were studied, three types of elastic configuration of the pulmonary trunk were described. Ac- cording to Heath et al., the presence of long elastic fibers, similar to those seen in the aorta, give the pulmonary artery of the fetus and newborn an "aortic " or " fetal " type of con- figuration. From the sixth month to the end of the second year the fibers appear frag- mented and this characterizes the " transi- tional" pattern. The scantiness and irregular- ity of the elastic tissue are the main histologic features of the so-called "adult'" type. We have studied the normal variations of the elastic configuration of the pulmonary trunk in a large series of cases comprising both sexes and of all ages. Some differences from the earlier concepts and facts not pre- viously referred to form the subject of the present report. For the understanding of the changes observed under abnormal conditions it is necessary to be familiar with these earlier concepts and the differences now to be de- scribed. Material and Method A total of 443 cases was studied. The ages varied from the first trimnester of intrauterine life to 94 years. There were 20 cases in the prenatal group, the youngest being a fetus of thie second month and From the Departmenit of Pathology, Faculty of Medicine "ICayetano Heredia," Universidad Peruana de Ciencias Medicas y Biol6gicas, Lima, Peru. Supported by U. S. Public Health Service Grants G-8576 and H-7000. the oldest a premature stillborn weighing 2,350 grams. Four hundred and twenty-three cases of both sexes, ranging in ages fronm birth to the tenth decade of life, were studied. The number of cases at different ages is indicated in table 1. The most frequent causes of death were acci- dents in adults and acute bronchopneumonic proc- esses in children. In the majority of these cases the postmortem studies were performed for medicolegal purposes at the Central Morgue of Lima. Cases from the Loayza Hospital and the Children's Hospital of Lima were also included. Great care was taken to discard cases with cardiac malformations or cardiovascular disease. In 43 cases of the first decade of life the intact hearts were obtained. In these cases, for reasons of a different study,2 the right and left ventricu- lar masses were separated and then the ratio left/ right ventricular weight (Herniann-Wilson index) 3 was obtained. This information has been taken into consideration in the interpretation of results. In the usual histologic preparations the elastic tissue of the media of the pulmonary trunk and the aorta appears in the form of fibers. It actu- ally constitutes sheets or laminae, the sites of "fragmentation" of fibers representing holes or fenestrations of laminae.4 These facts, in the case of the aorta, have been excellently illustrated by Elias.5 Some previous observations were carried out to verify these structural characteristics. In six cases, most of them less than 1 year of age, several cuts in differently oriented planes to the axis of both pulmonary trunk and ascending aorta were made. In every case, the appearance of the elastic tissue, in both arteries, was essentially the same in trans- verse, longitudinal, and oblique sections. This fact agrees with a lamellar disposition of elastic mate- rial in the arterial wall. However, some accentua- tion in the degree of fenestration of laminae could be frequently noticed in the longitudinal sections. To exclude minor changes ascribed to the plane of sectioning, the samples of arterial wall were always obtained from transversal planes of the anterior wall of the pulmonary trunk and right posterior wall of the ascending aorta, 2 to 3 cm. Circulation, Volume XXVII, June 1968 1086 by guest on February 11, 2018 http://circ.ahajournals.org/ Downloaded from
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Studies on the Structure of the Pulmonary TrunkI. Normal Changes in the Elastic Configuration of the
Human Pulmonary Trunk at Different Ages
By MARIO SALDANRA, M.D., AND JAVIER ARIAS-STELLA, M.D.
IN AN EARLIER study, Heath, Wood,DuShane, and Edwards' have pointed out
the morphologic characteristics of the elastictissue in the trunk of the pulmonary arteryin cases of congenital and acquired cardiopa-thies. Among 71 "control" cases that werestudied, three types of elastic configurationof the pulmonary trunk were described. Ac-cording to Heath et al., the presence of longelastic fibers, similar to those seen in the aorta,give the pulmonary artery of the fetus andnewborn an "aortic " or " fetal" type of con-figuration. From the sixth month to the endof the second year the fibers appear frag-mented and this characterizes the " transi-tional" pattern. The scantiness and irregular-ity of the elastic tissue are the main histologicfeatures of the so-called "adult'" type.We have studied the normal variations of
the elastic configuration of the pulmonarytrunk in a large series of cases comprisingboth sexes and of all ages. Some differencesfrom the earlier concepts and facts not pre-viously referred to form the subject of thepresent report. For the understanding of thechanges observed under abnormal conditionsit is necessary to be familiar with these earlierconcepts and the differences now to be de-scribed.
Material and MethodA total of 443 cases was studied. The ages
varied from the first trimnester of intrauterine lifeto 94 years.
There were 20 cases in the prenatal group, theyoungest being a fetus of thie second month and
From the Departmenit of Pathology, Faculty ofMedicine "ICayetano Heredia," Universidad Peruanade Ciencias Medicas y Biol6gicas, Lima, Peru.
Supported by U. S. Public Health Service GrantsG-8576 and H-7000.
the oldest a premature stillborn weighing 2,350grams.Four hundred and twenty-three cases of both
sexes, ranging in ages fronm birth to the tenthdecade of life, were studied. The number of casesat different ages is indicated in table 1.
The most frequent causes of death were acci-dents in adults and acute bronchopneumonic proc-esses in children. In the majority of these casesthe postmortem studies were performed formedicolegal purposes at the Central Morgue ofLima. Cases from the Loayza Hospital and theChildren's Hospital of Lima were also included.Great care was taken to discard cases with cardiacmalformations or cardiovascular disease.
In 43 cases of the first decade of life the intacthearts were obtained. In these cases, for reasonsof a different study,2 the right and left ventricu-lar masses were separated and then the ratio left/right ventricular weight (Herniann-Wilson index) 3was obtained. This information has been takeninto consideration in the interpretation of results.
In the usual histologic preparations the elastictissue of the media of the pulmonary trunk andthe aorta appears in the form of fibers. It actu-ally constitutes sheets or laminae, the sites of"fragmentation" of fibers representing holes orfenestrations of laminae.4 These facts, in the caseof the aorta, have been excellently illustrated byElias.5Some previous observations were carried out to
verify these structural characteristics. In six cases,most of them less than 1 year of age, several cutsin differently oriented planes to the axis of bothpulmonary trunk and ascending aorta were made.In every case, the appearance of the elastic tissue,in both arteries, was essentially the same in trans-verse, longitudinal, and oblique sections. This factagrees with a lamellar disposition of elastic mate-rial in the arterial wall. However, some accentua-tion in the degree of fenestration of laminae couldbe frequently noticed in the longitudinal sections.To exclude minor changes ascribed to the planeof sectioning, the samples of arterial wall werealways obtained from transversal planes of theanterior wall of the pulmonary trunk and rightposterior wall of the ascending aorta, 2 to 3 cm.
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above the valve. In most fetuses, newborns andinfants, the samples were taken fronm 0.1 to 1 cm.above the valves.
Tissues were fixed in 10 per cent form-alin andembedded in paraffin. Microscopic sections werecut at 6,u and stained for elastic tissue withfuchsin-resorein according to the Weigert technicand counterstained with Van Gieson's picro-fuchsin for connective and muscular tissues.6
The descriptions to be presented refer to struc-ture considered in one plane. So we will speak ofelastic fibers instead of laminae, fragmentation offibers rather than fenestration of laminae. It isalso necessary to distinguish true elastic fibersfrom numerous fibrils or filaments of the samematerial which mingled with the connective tissueand muscular bundles of the arterial wall.A "blind" study was performned. The sections
were labeled with a key number to prevent anyinformation in regard to the case during thestudy. Then, the type of elastic configuration ofthe pulmonary trunk was determined in everyinstance. Cases showing areas of different elasticconfiguration were classified according to the pat-tern present in the major part of the section.
ResultsPrenatal GroupWe have not been able to note any differ-
ence between the elastic configurations of thepulmonary trunk and the aorta in the courseof the wvhole fetal life.Even in the first trimester of intrauterine
life the abundance of elastic fibers in bothvessels is striking. These are thin, somewhatdiscontinuous, and show a winding, concen-tric course. Particularly in the inner portionof the arterial wall, the elastic fibers adopt areticular pattern surrounding muscular cells
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(fig. lA). During this period the elastic ma-terial takes less stain than after birth. It isnot always possible to distinguish a definiteinternal elastic lamina. An external elasticlamina is never observed.From approximately the fourth month the
thickness of the fibers increases, their tortuos-ity diminishes, and a well-defined paralleldisposition is noticeable (fig. 1B).
In the last 3 months of prenatal life theelastic configuration of the pulmonary arteryand aorta is similar to that observed in thenewborn.The different types of elastic configuration
adopted after birth by the pulmonary trunkwill now be briefly outlined. Emphasis willbe directed toward characteristics not previ-ously mentioned. A number of cases by agesand types of elastic configuration of the pul-monary trunk are presented in table 1. Theevolution of the elastic configuration of thepulmonary trunk in the course of postnatallife is illustrated in figure 2.
"Aortic" Type of Pulmonary Trunk
The pulmonary artery of the newborn showsa great content of long, straight or undu-lating, parallel and closely arranged elasticfibers, just as in the case of the last trimesterof intrauterine life. The designation of pul-mlonary artery of the "aortic" type given byHeath et al.1 is justified because of similaritywith its corresponding aorta (figs. IC and1D). On the other hand, it would not seem
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Figure 1A, upper left. Pulmonary trunk- of a fetus in thethird month of gestation shouwiug the pericellulararrangement of elastic mtaterial. X 750. B, upper
right. Pulmonary trunk of a fetus in the fifthmonth of gestation. Elastic fibers now display re-
markable parallelism. X 250. C, lower left. R.P.,
,,,I , I,I0 20 50 70 l00
Percent ot cases
Figure 2Changes in the elastic configuration of the normalpumnonary trunk in relation to age. See table 1.
precise to speak of "fetal" configuration,since there is not a single elastic pattern inthe course of intrauterine life.
The fibers of the pulmonary trunk show lessparallelism and regularity in thickness thanthose of the aorta. As noticed by Heath et al.,the degree of fragmentation of the fibers isapproximately the same in both arteries.The " aortic" configuration was observed
froni birth to the third month. It accountedfor 65 per cent of the cases in this period.The oldest case with the "aortic" type ofpulmonary trunk was a 3-month-old boy (fig.IC). In the 24 days following birth this wasthe only elastic configuration observed. Ninety-three per cent of "aortie" cases were in thefirst 29 days of life."Transitional" Type of Pulmonary Trunk
Heath et al.' described the fragmentationof the long fibers meintioned in the precedingtype as the main characteristic of this elasticconfiguration. However, our observations showthat not all of those fibers have fragmentation.Attention must be paid to the oceurrence of
a 3-month-old boy. Pulmonary trunk of "aortic"type. X 160. D, lower right. Same case as C.Ascending aorta for comparison. X 160. T-Veigert'sfuchsin-reso rcin stain for elastic tissue., counter-stained wvith Van Gieson's picro-fuchsin. In Athe nuclei wvere stained with TVeigert's ironht ematoxylin.
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disintegratory changes without reaching thepoint of fragmentation of the long fibers.Furthermore it is thought, based on the ex-
tent of fragmentation or disintegration, thattwo patterns or " transitional. models can be
Iigr 3distinguished. They are designated A and B."Transitional-A" Model. This model actu-
rne*tattno softfiesireiyn d Dally corresponds to Heath's et al. originaldescription for the "transitional" configura-tion. These cases exhibit a majority of clearlyfragmented fibers (figs. 3A and 3B). The re-
suiting fragments appear isolated. Many ofg ~~~~them swell and they may disintegrate formingi ~~~~elastotic masses.
The "transitional-A" model was observedfrom 25 days to 3 years. In this age range
*1*~~~~~ it represented 35 per cent of the cases. Ex-4 ~~~~~~~remeayes corresponded to a 25-day-old boy
(i.3)and to a 3-year-old girl.4 "~~~~~Transitional-B" Model. In cases with this
j~ elastic pattern what, in the majority of fibers,appears as zones of fragmentation, really cor-
tecompact elastic nucleus has been replacedbynumerous delicate elastic fibrils that main-tantecontinuity of the long fibers (figs. 3C,3 aid4C). These fibers can be considered
as partially disintegrated but not fragmented.Some fibers do show a real fragmentation.The "transitional-B" model was observed
between 1 month and 9 years. From 1 to 11months this model accounted for 27 per centof the cases and for 32 per cent of those inthe 1- to 9-year period. The youngest case
with the "transitional-B" model was a 1-month-old girl and the oldest case a 9-year-oldboy (fig. 3C)."Persistent" Type of Pulmonary Trunk
This designation has been applied to a typeof elastic configuration of the pulmonary
than that observed in A. X 16'0. C, lower left.Figure 3 G.O., a 9-year-old boy. Pulmonary trunk of "tran-
A, upper left. J.D., a 25-day-old boy. Pulmonary sitional-B" model. Delicate elastic filaments main-trunk of "transitional-A" model. A clear-cut frag- tamn the continuity of most of the fibers. X 160.mentation of most of the fibers is readily noticed. D, lower right. P.1V., a 5-year-old yirl. PulmonaryX 160. B, upper right. D.T., a 5-month-old girl, trunk of "1transitional-B" model, to show) the eon-Pulmonary trunk of "transitional-A"l model. A tinunity of the fibers through delicate elastic fila-more marked degree of fragmentation of fi-bers ments. X 160.
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riguA, upper left. M.M., a 5trunk of "persistent" typelastic fibers is striking.fragmeented. X 160. B, urold girl. Pulmonary truAn, undulating course of
trunk, which can be observed in the first 5years of life. Here, the pulmonary arteryshows such a content of elastic fibers that, atfirst sight, it looks like a ease of the "aortic"type (figs. 4A and 4B). However, a greaterdegree of fragmentation of fibers than thatseen in the "aortic" tvpe mnay be clearly de-tected.A combination of long, thick fibers, which
resemble those present in the "aortic" model,with others markedly fragmented, is the maincharacteristic of this elastic configuration.Long fibers are more numerous than frag-mrented ones. The density of the elastic con-tent confers a compact appearance to themnedia (figs. 4A and 4B).For this configuration the designation "per-
sistent" has been given because of the abun-daniee of long fibers, that are more character-istic of the last fetal period, or, at the most,the 3 months that follow birth.
X.-iw i The occurrence of a significant number of|ragmriented fibers makes the differenee be-
@ A | S i tweeni the ' persistent ' and the ' aortic" type.On the other hand, the presence of numerous
lorig fibers makes the distinction from the two''tranisitional" models. The richness in elasticmiiaterial prevents any possibility of confusionwith the "adult"' type.The " persistent " eonfiguration was ob-
served between 1 mnonth and a years in 19 perCent of the cases. The youngest case was a1-miolnth-old girl and the oldest ease a 5-year-old boy (fig. 4A). Most of the "persistent"cases belonged to the first 3 years of life, espe-cially to the first 11 months.
"Adult" Type of Pulmonary Trunk
As described by Heath et al., a poor coii-tent in elastic tissue is the main characteristicof this configuration. The majority of fibers
a greater part of the section. X 180. C, lower left.tre 4 Same case as B. It exhibited, in zones, a "transi--year-old boy. Pulmonary tional-B" model, as illustrated. This fact is evi-)e. The abundance of long dence that cases with the "persistent" type mayOther fibers are clearly evolve toward the "a,dult" type through the "'tran-
?per right. P.R., a 3-year- sitional-B" model. X 180. D, lower right. H.V., ank of "perststent" type. 2-year-and-5-month-old boy. Pulmonary trunk offibers was appreciated in "adult" type. X 160.
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are short, thin, and placed widely separatedby abundant fibromuscular tissue (fig. 4D1).A 12-month-old boy was the youngest case
that exhibited the "adult" type of pulmonarytrunk. Over the ninth year this elastic typewas the only one observed.
DiscussionMost of the changes in the elastic structure
of the pulmonary trunk can be interpreted inthe light of current physiologic information.According to Heath et al., the "aortic"
type is associated with the pulmonary hyper-tension present in the newborn.7 A greatcontent of long elastic fibers allows a vesselof small diameter to tolerate a mean bloodpressure of about 35 mm. of mercury.8' 9 Thefact that high pressure determines and main-tains this type of elastic configuration is con-firmed by the finding of examples of "aortic"configuration, even in adult life, in cases ofcongenital cardiopathies associated with pul-monary arterial hypertension from birth.'When performing right heart catheteriza-
tion studies in children with normal cardio-vascular systems, Rowe and James9 foundthat from the second week of life the pressurein the trunk of the pulmonary artery hadalready fallen to 16 mm. of mercury (meanpressure). If we accept that high pulmonaryarterial pressure is the mechanical stimulusthat maintains the integrity of the fetal fibers,then the zonal fibrillary disintegration andfragmentation of elastic fibers observed in the"transitional" models might be brought aboutby the sudden fall of pulmonary arterial pres-sure that occurs after birth. The partial frag-mentation of fibers noticed in the "persistent"type could also be related to this same cause.However, nothing conclusive can be stated
at present with reference to the exact physio-logic significance of each of the above-men-tioned elastic configurations. This is due tothe lack of specific hemodynamic information,an almost unsurmountable obstacle. Neverthe-less, some insight into the problem can be in-directly gained by studying the left/rightventricular weight ratios in a group of thesecases.
As indicated, in 43 cases ranging in agesfrom 4 months to 9 years, the right and leftventricular masses were dissected, and theHermann-Wilson index, which relates theweight of the latter to that of the former, wasobtained.3 In the group of cases in which theHermann-Wilson index was determined, the*transitional-A," "transitional-B," "persist-ent,' and "adult' elastic patterns were pres-ent. In no one of these cases was the left/right ventricular weight ratio out of the nor-mal range (fig. 5). This fact adds support tothe consideration that all of the above-men-tioned types are normally occurring forms ofevolution of the elastic configuration of thepulmonary trunk.According to ages and to type of elastic
configuration these cases were distributed intwo groups: from 4 months to 3 years, groupI; from 3 to 9 years, group II.
In group I the mean values for the left/right ventricular weights ratio were 1.70 for"'persistent" cases, 2.04 for "transitional-A"cases, and 1.84 for "transitional-B" cases.The difference between mean values of "per-sistent" and "transitional-A" cases was sta-tistically highly significant (p < 0.001). Nosignificant statistical difference was encoun-tered on comparing "persistent" versus"transitional-B" mean values (p < 0.10) or" transitional-A " versus "transitional-B"mean values (p < 0.70).
In group II, the mean value of the Her-
2.20-2.10 0- ..__. _2.00- 08 o 01.901.80-*1.70 - 0
mann-Wilson index was 1.74 for " transi-tional-B" cases and 1.88 for "adult" cases
(p < 0.05).With the foregoing informatiomi a correla-
tion between changes in the elastic configura-tion of the pulmonary trunk, the Hermann-Wilson index values, and hemodynamicphenomena has been attempted. An interpre-tation of the histogenetic evolution of theelastic configuration of the pulmonary trunk,based on this reasoning, is proposed in fig-ure 6.A great content of long elastic fibers and
significant lower values of the Hermann-Wil-son index, as observed in "persistent" cases,would be in relation to a postnatal fall ofpulmonary pressure detained at the highestlevels of normality.The marked fragmentation of elastic fibers
and the highest normal values of the Her-
a (Birth - 3mth)
A (1-96yr)Figure 6
Pathways of normal histogenetic evolution of theelastic configuration of the pulmonary trunk; a,"aortic"'; P, persistent; TB, transitional-B" model;TA, "transitional-A" model: A, "ladult" type. Theage ranges of these types are in parentheses.
manrn-Wilson index observed in eases with the" transitional-A" model, can perhaps be ex-plained by a pronounced postnatal fall ofpulmonary pressure, which reaches to thelowest levels of normality.
In the first 3 years of life, " transitional-B"cases would correspond to pulmnonary pressurelevels between those that determine the " per-sistent " type and " transitional-A "' model.From 3 to 9 years, " transitional-B " caseswere found to have values significantly lowerin the Hermann-Wilson index than in caseswith the "adult" type of pulmonary trunk.This finding suggests that, in this period, theyeorrespond to the higher normal figures ofpulmonary pressure. It may be that some ofthese cases actually represent an advancedstage of the "persistent " configuration, assuggested by the almost equal values in theHermann-Wilson index. The fact that afterthe eleventh month of life, the proportioni of"transitional-B" cases increase while "per-sistent" cases become m-ore scarce (table 1)would favor this possibility. Furthermore,the "transitional-B" pattern has been occa-sionally observed in zones of cases of the"persistent" configuration (figs. 4B and 4C).
Finally, according to Heath et al., the"adult" type of pulmonary trunik is relatedto the low level of arterial pressure normiallyexisting in the lesser circuit; a highly richelastic aortic media reflects a pressure five tosix times greater in the systemic circulation.
SummaryA study of the elastic configuration of the
pulmonary trunk was undertaken in 443 nor-mal autopsy cases, ranging in ages from thesecond month of intrauterine life to 96 years.
It has been shown that during the whole offetal life the elastic configuration of the pul-monary trunk is similar to that observed inthe ascending aorta.The "aortic" configuration of the pulmo-
nary trunk, which is characterized by a greatcontent of long elastic fibers, was observed inthe first trimester of life, especially in the 29days that follow birth.Two models of the "transitional" config-
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uration have been distinguished. The "transi-tional-A" model is characterized by a markedfragmentation of the elastic fibers. This elas-tic pattern has been found between 25 daysand 3 years. In the " transitional-B" modelmost of the fibers are partially disintegratedbut not fragmented. Cases with this charac-teristic were found from 1 month to 9 years.The "adult" type of pulmonary configura-
tion, which exhibits a poor content in elastictissue, was already present in the twelfthmonth of life. Over the ninth year it consti-tuted the totality of cases.A fourth elastic configuration has been
added to the already known "aortic, " "tran-sitional," and "adult" types. The designa-tion of "persistent" given to this elastic typealludes to the presence of numerous long elas-tic fibers that are more characteristic of the"aortic" type, alternating with others thathave suffered fragmentation. Cases of the"cpersistent" type were found from 1 monthto 5 years.A hemodynamic interpretation of the
changes observed in the "transitional" mod-els and "persistent" configuration is pro-posed.
AcknowledgmentThe valuable suggestions and criticisms of Dr.
Averill A. Liebow are gratefully acknowledged. Wealso express our thanks to Dr. Sixto Recavarren, whokindly allowed us the use of his data on ventricularweights; and to Dr. Ramon Criado, Director ofthe Central Morgue of Lima, and to Dr. Gerardo
Boisset from the Children 's Hospital of Lima forthe use of their anatomic material.
References1. HEATH, D., WOOD, E., DUSHANE, J., AND
EDWARDS, J.: The structure of the pulmonarytrunk at different ages and in cases ofpulmonary hypertension and pulmonary steno-sis. J. Path. & Bact. 77: 443, 1959.
2. ARIAS-STELLA, J., AND RECAVARREN, S.: Rightventricular hypertrophy in native children liv-ing at high altitude. Am. J. Path. 41: 55, 1962.
3. HERMANN, G. R., AND WILSON, F. N.: Ventricularhypertrophy: A comparison of electrocardio-graphic and post-mortem observations. Heart9: 91, 1921.
4. HAM, W. A.: Histology. Ed. 3. Philadelphia,J. B. Lippincott Company, 1957, 485 pp.
5. ELIAS, H.: The structure of blood vessels.In Luisada, A: Cardiology (An Encyclopediaof the Cardiovascular System). New York,McGraw-Hill Book Company, Inc., 1959, vol.1, P. 191.
6. LILLIE, R. D.: Histopathologic Technic andPractical Histochemistry. Ed. 2. New York,McGraw-Hill Book Company, 1954, pp. 361and 346.
7. ADAMS, F. H., AND LIND, J.: Physiological studieson the cardiovascular status of normal newborninfants (with special reference to the ductusarteriosus). Pediatrics 19: 431, 1957.
8. RUDOLPH, A. M., DRORBAUGH, J. E., AULD,P. A. M., RUDOLPH, A. J., NADAS, A. S.,SMITH, C. A., AND HUBBELL, J. P.: Studieson the circulation in the neonatal period.The circulation in the respiratory distress syn-drome. Pediatrics 27: 551, 1961.
9. RoWE, R. AND JAMES, L. S.: The Normal pul-monary arterial pressure during the first yearof life. J. Pediatrics 51: 1, 1957.
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