Thorax (1952), 7, 249.

AN ABNORMAL DISPOSITION OF THE PULMONARY VEINSBY

H. BUTLERFrom the Department of Anatomy, St. Bartholomew's Hospital Medical College, London

(RECEIVED FOR PUBLICATION DECEMBER 10, 195 1)

The entrance of the pulmonary veins into theright atrium or into the systemic veins is suffi-ciently uncommon, but rarer still is their entranceinto the portal venous system. Since the firstexample of abnormal disposition of the pulmonaryveins was described by Winslow in 1739 theliterature reveals reports of 138 instances con-firmed at necropsy (Brody, 1942; Hughes andRumore, 1944; Brantigan, 1947; Young, 1947;Edwards and DuShane, 1950; Edwards, DuShane,Alcott, and Burchell, 1951 ; Smith, 1951). Recentlyadditional examples have been diagnosed byangiocardiography and cardiac catheterization(Welti and Nedey, 1950; Hwang, Prec, Kuramoto,Segall, and Katz, 1950; Runstrom and Sigroth,1950; Grishman, Brahms, Gordon, and King,1951), but because they lack direct anatomicalconfirmation they are not here considered further.While anomalies of the systemic veins arenotoriously frequent, recorded anomalies of thepulmonary veins are remarkably few. It will beshown here that the mode of development of thepulmonary vein is such that the incidence of itsanomalies might be expected to exceed thatrecorded.Twelve of the 138 anatomically confirmed

examples showed abnormal pulmonary veins whichentered, totally or partially, the portal venoussystem. In eight such instances the pulmonaryveins drained into the stem of the portal vein(Ramsbotham, 1829; Bochdalek, 1858; Geipel,1899; Hu, 1929; Munck, 1933; Terplan andSanes, 1936 ; Young, 1947; Mykschowszky, 1948);in three instances they drained into the left branchof the portal vein via the still patent ductusvenosus (Ghon, 1916; Mehn and Hirsch, 1947;Edwards and DuShane, 1950); in Arnold's (1868)specimen, of intermediate type, the pulmonaryveins were connected to the obliterated ductusvenosus, the left branch of the portal vein, thestem of the portal vein, and directly to the intra-hepatic veins of the quadrate hepatic lobe. Thepersonal specimen described below is an exampleof a common pulmonary vein joining the left

branch of the portal vein close to the beginning ofthe ductus venosus.

SUMMARY OF THE CASE HISTORYA second child, born at 9.15 p.m. on January 25,

1951, after an uneventful pregnancy, appeared to benormal, but became pale and collapsed three and ahalf hours later. After extraction of mucus and theadministration of oxygen some colour returned, butthe child remained cyanosed until his sudden deathat 6.45 p.m. on January 26-that is, 451 hours afterbirth.

POST-MORTEM REPORTThe body is that of a moderately well nourished

newborn male infant with conspicuous cyanosis,particularly of the extremities.The lungs are poorly aerated, but apart from the

generalized congestion of the various organs, the onlyabnormalities present are those of the pulmonary veinsand of the left side of the heart.Three pulmonary veins issue from the right lung

and two from the left: these join to form, respec-tively, short, wide right and left pulmonary veinslying on the anterior aspect of the oesophagus outsidethe pericardium. The right and left pulmonary veinsimmediately unite into a common pulmonary vein,2.5 cm. long and 4.0 mm. in diameter, lying on theoesophagus close to the right vagus nerve (Fig. 1).This common pulmonary vein runs caudally, just to

, Pul. V.

FiG. 1.-Drawing of the heart, lungs, and oesophagus showing. the commonpulmonary vein and the abnormal intrapericardial folds. For key, see Fig. 6.

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H. BUTLER

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FIG. 2.-Drawing of the liver as seen from below and behind showing the termina-tion of the common pulmonary vein. A window has been cut in the terminalpart of the common pulmonary vein to show the site of the stenosis dueto the proliferating connective tissue. The caudate and part of the lefthepatic lobes have been removed. For key, see F-ig. 6.

the left of the midline, to pierce the diaphragmthrough an adventitious foramen situated, betweenthe oesophageal and caval foramina. It then runsin the left triangular ligament, passing immediatelyposterior to the left hepatic vein to run in the groovebetween the hepatic caudate and sinistral lobes. Hereit lies parallel to, and to the left of, the still-patentductus venosus. It terminates in the left branch ofthe portal vein, by a narrow orifice, immediately tothe left of the ductus venosus and almost oppositethe still-patent intra-abdominal umbilical vein (Fig. 2).The narrowing of its terminal orifice, which is lessthan 1.0 mm. in diameter, is due to thickening of thevessel wall.

The "T "-shaped vessel .^ .formed by the right, left, -and common pulmonary .. '.veins is closely applied tothe exterior of the fibrouspericardium immediatelycaudal to the base of theheart. Within the pert-cardial cavity appear twocrescentic folds of theserous pericardium. Thesebegin on the uppermostpart of the dorsal wallof the pericardial sac atthe level of the right and r rleft pulmonary veins, crossthe line of the pericardial ~i.reflection, and thereafterrun on to the posteriorsurface of the left atrium.Here they run caudally,gradually approaching eachother, to fade away at thelevel of the junction of the FIG. 3.-An oblique sect

proliferating conne4inferior vena cava and right stain, x 50. For I

atrium (Fig. 1). Owing to the absence of the intra-pericardial parts of the pulmonary veins the obliquesinus is only imperfectly formed, and these foldsform its incomplete left boundary. The right foldis avascular, but the left contains a leash of smallveins connecting the left upper pulmonary vein to theleft atrium. These small veins and the Thebesianveins are the only vessels entering the left atriumapart from the via sinistra of the inferior vena cava.The respective capacities of the left atrium and

ventricle are estimated to be less than half those oftheir right counterparts. There is little difference inthickness of wall between the right and left cardiacchambers, but the left ventricular wall is very slightlythe thinner. The aorta, pulmonary arteries, and venaecavae are normal: the foramen ovale is patent butvalvular.The distal end of the common pulmonajy vein and

the ductus venosus were serially sectioned at 10 I',and alternate slides were stained with Weigert-VanGieson's stain and with haematoxylin and eosin.Examination showed the last 3 mm. of the commonpulmonary vein to be narrowed by the ingrowth of amass of newly formed, vascular, connective tissuemost prolific at the termination of the vein, whoselumen was thereby reduced to a diameter of less thanI mm. About 1 mm. from the vein mouth theamount of newly formed connective tissue decreasedabruptly, and thereafter more gradually faded awayto end some 3 mm. along the vessel. This new tissueconsisted of fibroblasts with large, elongated, vesicu-lar nuclei, a number of which were undergoing mitoticdivision. The ground substance showed no redcoloration with van Gieson's stain. Scattered amongthe fibroblasts were a few small, irregularly arrangedelastic fibres and an occasional plasma cell. The wall

.1

A,;' '.

I;

S-. . .'F.j,9.t.- a- .\ ..

tion through the terminal part of the common pulmonary vein showing the:ctive tissue encroaching on the vessel lumen. Weigert-van Gieson'skey, see Fig. 6.

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AN ABAORMAL DISPOSITION OF THE PULMONARY VEINS

of the common pulmonary veinwas 900 IA thick and consisted Kof collagen fibres, longitudinalsmooth muscle, and numerous V.

coarse elastic fibres (Figs. 3and 4).The ductus venosus wall was

thinner (480 pA), and consisted \ fmainly of collagen fibres with % fsome coarse elastic fibres and P f hta few longitudinal smooth /muscle fibres. It, too, wasundergoing initial obliteraticnthroughout its entire length bynewly formed vascular connec-tive tissue, precisely similar tothat within the common pul- 7-pmonary vein. This adventitiousconnective tissue was mostabundant at the site of unionwith the portal vein. Similar,but much less abundant, tissuewas found in the terminal part FIG. 4.-A high-powerof the intra-abdominal umbili-cal vein.Liver sections showed congestion of the sinusoids

and the presence of large fat globules within thehepatic cells.

DISCUSSIONThe specimen described above closely resembles

those recorded by Ghon (1916), Mehn and Hirsch(1947), and Edwards and DuShane (1950), andconstitutes the fourth known example of this par-ticularly rare venous anomaly. Two types of

C. rul. v.,. , Oes.

.4.i t'4

view of the newly formed, vascular connective tissue. Haematoxylin andeosin, x 360.

anomalous entrance of the pulmonary veins intothe portal venous system can be recognized (Fig.5). Type A includes the above-mentioned casesand is characterized by the union of all the pul-monary veins into a single common pulmonaryvein which runs caudally, in close contact withthe oesophagus, and generally perforates thediaphragm through an adventitious foramensituated between the oesophageal and caval for-amina, but exceptionally (Edwards and DuShane,1950) traversing the oesophageal hiatus. Below

I.V.C. C.Pul.V. Oes.. .~~~~~~~~~~~~~~~~~

TYPE A TYPE BFIG. 5.-Diagram to illustrate the two types of pulmo-portal venous anomalies. For key, see Fig. 6.

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H. BUTLER

the diaphragm the common pulmonary vein runsin the groove on the left side of the hepatic caudatelobe to join the left branch of the portal vein, via,or close to, the still-patent ductus venosus.Clinically, all patients suffering from this disabilitymanifest cyanosis and die early (Table I). Only

TABLE IPULMO-PORTAL VENOUS ANOMALIES TYPE A

A Age at Associated MajorAuthor Death Cardiac Anomaly

Ghon (1916) .. 15 days NoneMehn and Hirsch (1947) 12 ,, Coarctation of the aortaEdwards and DuShane (1950) 9 NonePresent case .. 45 A hours

.

FIG. 6 -A typical example of type B pulmo-portal venous anomaly(reproduced from Bochdalek, 1858).

C.T. = newly forn.ed connective tissue. D. Ven. = ductus venosus.Diaph. = diaphragn.. Elast = elaistic tissue in wall of commonpulmonary vein. L.Gcst V. = left gastric vein. R.Hep. V. =right hepatic vein. L.Hep. V. = left hepatic vein. 1. V.C. = inferiorvena cava. Oes. = oesophagus. PeriC. = cvt edge of peri-cardium. PeriF. = anomalous intrapericardial folds. Port. V.stem of portal vein. R.Port.V. right branch of portal vein.L.Port. V. = left branch ofportal vein. C.Pul. V. =common pul-monary vein. R.Pul. V. =right pulmonary vein. L.Pul. V. = leftpulmonaryv vein. Ufmb. V.= intra-abdominal umbilical vein. Vag.=lagus nerve. Ao. = aortai.

one example (Mehn and Hirsch, 1947) showed anassociated major cardiac anomaly.

Eight recorded examples of anomalous pul-monary vein arrangement presented the pattern ofa common pulmonary vein running caudally withthe oesophagus, and, in five instances, piercing thediaphragm via the oesophageal hiatus (Rams-botham, 1829; Bochdalek, 1858; Geipel, 1899:Hu, 1929; Munck, 1933; Terplan and Sanes.1936; Young, 1947; Mykschowszky, 1948). Sucha common pulmonary vein joins the stem of theportal vein via the grossly dilated terminal part ofthe left gastric vein behind the peritoneal posteriorwall of the lesser sac. These examples constitutetype B of anomalous pulmo-portal venous arrange-ment, which is well illustrated by the specimendescribed by Bochdalek (1858) (Figs. 5 and 6).Patients manifesting type B anomaly suffer fromcyanosis and, despite the fact that the majority ofthem present an associated major cardiac anomaly,live longer than patients with type A anomaly(Table II).

TABLE 11I ULMO-PORTAL VENOUS ANOMALIES TYPE B

Author Age at Associated MajorDeath Cardiac Anomaly

Ramsbotham (1829) 6 mths Cor biloculareBochdalek (1858) 4 days I.V.C. enters both atriaGeipel(1899). .. 3-6 mths R. half of a thora-

I.U.L. copagusHu (1929) . .. 7 ., Cor triloculare, etc.Munck (1933) 3 ,, NoneTerplan and Sanes (1936) 12 hours Cor triloculare biatri-

atrium. etc.Young (1947) .. . Born dead Cor biloculareMykschowszky (1948) 18 days None

Arnold's (1868) specimen is of considerableinterest, in that the connexions of the pulmonaryvein exhibit features of types A and B and,additionally, direct connexions with the intra-hepatic veins of the quadrate lobe. Ramsbotham's(1829) specimen also showed a composite termin-ation of the pulmonary veins, the right vesselsjoining the portal vein, the left vessels the left sub-clavian vein.

It seems certain that the pulmonary vein has adual developmental origin, and, on such a hypo-thesis, an explanation of these anomalies may beoffered. Brown (1913) showed in the cat that theperipheral part of the pulmonary venous systemdevelops from that part of the foregut venous plexussurrounding the developing lung buds. The foregutvenous plexus develops in sitli in the splanchnicmesoderm and drains primarily into the heart viathe vitello-umbilical and cardinal veins. Only ata relatively late stage (8 mm. human embryo,

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AN ABNORMAL DISPOSITION OF THE PULMONARY VEINS

5.5 mm. cat and rat embryos) does it acquire an

independent and direct route into the heart by a

single pulmonary vein running in the caudal partof the dorsal mesocardium. Brown (1913) believedthat this connexion with the heart is due to theforward growth of the lung bud bringing the pul-monary part of the foregut venous plexus intocontact with the heart. Later investigators (Buell,1922; Schornstein, 1931; Chang, 1931; Streeter,1945; Auer, 1948; Butler, 1952) have shown thatan endothelial outgrowth from the dorsal wall ofthe sinu-atrial chamber of the heart unites with one

of the capillaries of the pulmonary part of theforegut venous plexus. Federow (1910) firstdescribed this endothelial outgrowth from theheart, but he believed that it gave rise to the wholeof the pulmonary venous system and not merelyto the stem of the pulmonary vein. Should thisunion fail, pulmonary venous outflow must, inorder to maintain the circulation, reach the heartby alternative routes such as are readily availablein the primary drainage routes of the foregutvenous plexus (i.e., the cardinal and vitello-umbilical veins). Thus, in the absence of a normalpulmonary vein, the pulmonary venous bloodreturns to the heart via the systemic or the portalvenous systems, including the ductus venosus.

Examples of all types of such anomalous venous

return have been described, but those utilizing theportal venous system are the most uncommon,

particularly those taking advantage of the ductusvenosus.

At an early stage the foregut venous plexusforms well-marked, longitudinal channels groupedaround the vagus nerves, the perivagal veins(Butler, 1952) which receive blood from theoesophagus and from the lung buds and drain intothe cardinal and vitello-umbilical veins; the closeassociation of the common pulmonary vein withthe vagus nerves in the case here describedstrongly suggests that these perivagal veins are

utilized to form the abnormal common pulmonaryvein. Further, in the human adult, the mostcaudal perivagal veins are the oesophagealtributaries of the left gastric vein (Butler, 1951)which enter the left gastric vein at the beginningof its retro-peritoneal portion, i.e., where the com-

mon pulmonary vein joins the dilated left gastricvein in examples of type B. In the adult rat theperivagal veins establish a direct connexion be-tween the left gastric vein and the pulmonary veins(Butler, 1952), and similar, but indirect, con-

nexions have been shown in man (Zuckerkandl,1882; Konaschko, 1929). It is also noteworthythat, in a number of specimens, the anomalous

R

common pulmonary vein traverses the oesophagealhiatus.

Little information is available regarding thedetails of ductus venosus development, the ductusbeing usually regarded as a derivative of thehepatic sinusoids. In the early stage of develop-ment the peri-gastric part of the foregut venousplexus has direct connexions with the hepatic sinu-soids (Butler, 1952), and such connexions maybe the means whereby an anomalous commonpulmonary vein may establish communication withthe ductus venosus. Such a view is supported byArnold's (1868) specimen which combined featuresof types A and B in that the common pulmonaryvein joined both the portal vein and the ductusvenosus and had, additionally, direct communica-tion with the intra-hepatic veins. In some instancesthe abnormal common pulmonary vein pierces thediaphragm by a separate foramen situated inmuch the same position as the left venous foramenof Blair (1923). Frequently Blair's foramentransmits a vein connecting the oesophageal veinsto the left hepatic vein and thus, indirectly, withthe ductus venosus. Blair (1923) regarded thisanastomotic vein as the remnant of the supra-hepatic part of the vitello-umbilical veins. Itmay well play a part in the formation of anomalouspulmonary veins of the pattern described here.Ramsbotham's (1829) specimen is of interest inshowing the pulmonary venous return utilizingboth primary drainage routes of the pulmonarypart of the foregut venous plexus, that is, systemicand portal veins, in the absence of a direct pul-monary venous connexion with the left side ofthe heart. Thus, all the potential routes for thepulmonary venous return demonstrable in theembryo and adult may be utilized, singly or incombination, when the pulmonary vein outgrowthfails to join the future pulmonary venous plexus.In the specimen described here the small veins inthe pericardial folds bounding the maldevelopedoblique sinus may represent an abortive attemptto form the stem of a normal pulmonary vein. Itis not possible to advance any plausible hypo-thesis for the failure of union of the pulmonaryvein outgrowth with the pulmonary venous plexus,but such a developmental error might reasonablybe expected to provide the basis for frequentanomalies of pulmonary venous pattern.The diversion of the pulmonary venous blood

from the left side of the heart does not appear toaffect the development of the embryo except in sofar as the reduced blood volume entering the leftatrium leads to a diminution of atrial capacitywhich in turn reduces left ventricular capacity.

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H. BUTLER

Such diversion is not necessarily associated withother major cardiac anomalies and its effectbecomes apparent only after birth. The diversionof the oxygenated blood leads to cyanosis and, ifcomplete, to early death (Brody, 1942).A striking feature of the present specimen is

the presence of proliferating connective tissue inthe terminal part of the abnormal common pul-monary vein. This tissue is identical with thatresponsible for the post-natal obliteration of theductus venosus and of the intra-abdominal umbili-cal vein, while similar tissue is also found in theobliterating ductus arteriosus. Its presence in thecommon pulmonary vein suggests that the terminalsegment of this vein was, in fact, a part of theductus venosus or that the obliterative process hadspread from the ductus venosus. This terminalstenosis must have seriously impeded the pulmon-ary venous return and may well have been partlyresponsible for the early death of the infant.Reference to Tables I and II shows that life isconsiderably shorter in those patients in whomthe abnormal common pulmonary vein opens intothe ductus venosus, despite the fact that type Bcases show a higher proportion of associatedmajor cardiac anomalies. Early obliteration ofthe terminal segment of the abnormal commonpulmonary vein, as described above, may accountfor this difference.

SUMMARYA specimen, the fourth to be recorded, is

described of an anomalous common pulmonaryvein draining into the left branch of the portalvein, close to the beginning of the ductus venosus.An embryological explanation, based on the

hypothesis of dual developmental origin of thepulm6nary vein, that is, from the heart and theforegut venous plexus, is submitted.The terminal part of the anomalous common

pulmonary vein was almost completely obliteratedby proliferatinfg connective tissue such as isnormally responsible for the obliteration of theductus venosus.

An attempt is made to classify the recordedexamples of pulmo-portal venous anomalies.

My thanks are accorded to Dr. A. M. Barrett, of theDepartment of Pathology, University of Cambridge,both for the presentation of this specimen and forpermitting its publication, and to Professor A. J. E.Cave for assistance in the preparation of this paper.To the departmental technicians, Miss J. Stedman andMr. A. E. Westwood, are due respectively the sectionsand the photomicrographs.

REFERENCES

Arnold, J. (1868). Virchows Arch., 42, 449.Auer, J. (1948). Anat. Rec., 101, 581.Blair, D. M. (1923). J. Anat., Lond., 57, 203.Bochdalek, V. A. (1858). Vjschr. prakt. Heilk., 60 (Jahrg. 15,

4), 160.Brantigan, 0. C. (1947). Surg. Gynec. Obstet., 84, 653.Brody, H. (1942). Arch. Path., Chicago, 33, 221.Brown, A. J. (1913). Anat. Rec., 7, 299.Buell, C. E. (1922). Contr. Embryol. Carneg. Instn (No. 66), 14, 1 1.Butler, H.(1951). Thorax, 6, 276.- (1952). J. Anat., Lond., 86, 95.Chang, C. (1931). Anat. Rec., 50, 1.Edwards, J. E., and DuShane, J. W. (1950). Arch. Path., Chicago,

49, 517.- Alcott, D. L., and Burchell, H. B. (1951). Ibid., 51,

446.Federow, V. (1910). Arb. Anat. Ir.st., Wiesbaden, 40, 529.Geipel, P. (1899). Festschr. Fiitfz-igjihren Bestehe' des Staatkranken-

hauses zu Dresden. Quoted by Ghon, 1916.Ghon, A. (1916). Beitr. path. Anat., 62, 175.Grishman, A., Brahms, S. A., Gordon, A., and King, F. H. (1951).

J. Mt Sinai Hosp., 17, 336.Hu, C. H. (1929). Amer. J. Path., 5, 389.Hughes, C. W., and Rumore, P. C. (1944). Arch. Path., Chicago,

37, 364.Hwang, W., Prec, O., Kuramoto, K., Segall, S., and Katz, L. N.

(1950). Circulation. 2, 553.Konaschko, P. 1. (1929). Z. Anat. EntwGesch., 89, 672.Mehn, W. H., and Hirsch, F. E. (1947). Amer. J. Path., 23, 125.Munck, W. (1933). Acta path. microbiol. Scand., 10,447 (erroneously

numbered 321).Mykschowszky, G. (1948). Klin. Med., Wien, 3, 263.Ramsbotham, F. (1829). London med. phys. J., 61 (n.s. 6), 548.Runstrom, G., and Sigroth, K. (1950). Acta. med. scand., Suppl.

246, p. 176.Schornstein, T. (1931). Morph. Jb., 67, 566.Smith,J. C.(1951). Amer. Heart S., 41, 561.Streeter, G. L. (1945). Contr. Embryol. Carneg. Instn (No. 199),

31, 29.Terplan, K., and Sanes, S. (1936). J. tech. Methods, 15, 86.Weld, J. J., and Nedey, R. (1950). Arch. Mal. Ceur, 43, 464.Winslow, J. B. (1739). Quoted by Brody (1942).Young. M. 0. (1947). Arch. Path., Chicago, 44, 169.Zuckerkandl, E. (1882). S.B. Akad. Wiss. Wien, 84, (abt. 3), 110.

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