A Histological Study of Surgical Landmarks for the Specialized Atrioventricular Conduction System, with Particular Reference to the Papillary Muscle

A Histological Study of Surgical Landmarks for the Specialized Atrioventricular Conduction System, with P d d a r Reference to the Papillary Muscleg Tatsuo Tamiya, M.D., Toshiyuki Yamashiro, M.D., Takafumi Matsumoto, M.D., Shohei Ogoshi, M.D., and Harumichi Seguchi, M.D. ABSTRACT Surgical landmarks of the conduction system were histologically evaluated in 29 cardiac specimens. The distribution of the system was grossly inherent to the type of ventricular septal defect as classified by Soto and coworkers, although it varied individually. The relationship of the right bundle branch (RBB) to the papillary muscles was of surgical interest. In defects unrelated to maldevelopment of the septum of the conus, the RBB passed beneath or slightly anterior to upper accessory papillary muscles (AcPMs) and posterior to the medial papillary muscle (MPM), regardless of the subtype of defect. In defects caused by maldevelopment, such as tetralogy of Fallot, it passed anterior to the MPM. Such data support the hypothesis that the RBB descends beneath or anterior to embryological upper AcPMs, whatever the morphological role may be, because of the supposedly independent developmental origin of the MPM and AcPMs. The relationship between the RBB and upper AcPMs appeared further modified by the attitude of the trabecula septomarginalis. Our improved clinical results have demonstrated that such information offers a gross but practical guide for prevention of conduction disturbances. Conduction disturbances introduced by intracardiac repair of congenital heart disease [l-31 remain an unsolved problem. The primary objective of our studies was to determine the precise topographical relationship of the conduction system to the intracardiac structure, thereby establishing intraoperative landmarks for prevention of such complications. The course of the bundle of His has been fairly well clarified to date, but that of the right bundle branch (RBB) has received far less attention [4-lo]. Of great surgical importance in the clarification of the course of the RBB should be the anatomical and embryological implication [ll, 121 that the RBB is the direct continuation of the His bundle. The specialized atrioventricular (AV) conduction system was histologically identified in 29 cardiac speciFrom the Second Departments of Surgery and Anatomy, Kochi Medical School, Kochi, japan. Presented at the Eighty-fourth Annual Congress of the Japan Surgical Society, Kyoto, Japan, Mar 29, 1984. Accepted for publication Feb 11, 1985. Address reprint requests to Dr.Tamiya, Second Department of Surgery, Kochi Medical School, Okocho, Nankoku, Kochi Prefecture 781-51, japan.

599

mens. In this report, particular attention is paid to the topographical relationship between conduction tissues and papillary muscles of the right ventricle, since our studies have demonstrated the existence of a pattern for both structures that may play the role of surgical guide in locating conduction tissues, particularly the RBB.

Material and Methods The 29 specimens used consisted of 4 normal hearts, 12 hearts with ventricular septal defect (VSD), 1 with complete AV septal defect, 7 with tetralogy of Fallot, 2 with truncus arteriosus, and 3 with transposition of the great arteries (TGA). All but 3 normal hearts and 1 malformed heart were from children ranging from 1 month to 7 years old (average age, 12 months). All hearts were studied by 10-p,m serial section technique, usually across the His bundle at an obtuse angle, followed by staining with Masson-Goldner or Van Gieson’s stain or both and a subsequent stereographic reconstruction of the specialized AV conduction system.

Anatomical and Terminological Remarks We use the VSD classification scheme of Soto and coworkers [13] in our anatomical description because of its adequacy. As for terminology, that of Anderson and Becker [141 has been employed preferentially throughout; with reference to the papillary muscle, however, we have been compelled to make a few provisional adaptations to describe the topographical relationship as precisely as possible. The term medial papillary complex used by Wenink [15] would be the most appropriate for the papillary muscle of the conus, which has also been referred to as the muscle of Lancisi or medial papillary muscle. But because of its vast morphological variations [15, 161 and because of our need to establish certain surgical landmarks, we have settled on a tentative scope of the medial papillary complex based on the description of Anderson and Becker (141 with a few additions of our own, as shown in Figure 1. Here the complex involves the papillary muscle or muscles that attach the posterior limb of the trabecula septomarginalis (TSM) to the portion of the tricuspid valve that includes the medial part of the anterior leaflet, the commissure leaflet, and the part of the septal leaflet anterior to the membranous septum. When the complex comprises two or more papillary muscles, we refer to the most anterior muscle as the medial papillary muscle (MPM), merely to point out the surgical landmark. The accessory (or septal)

600 The Annals of Thoracic Surgery Vol 40 No 6 December 1985

commissure cord

a part of septa1 Ieafle

memb. septum

(upper) septa1 pap. muscles

t

S;

pap. complr! X *

uppermost access pap

(lower) septa1 pap. muscles

/

Fig I . Nomenclature and definition of the papilla y muscles that join the tricuspid valve. See text for detailed explanation. (memb. = membranous; access. pap. = accessoy papillary; TSM = trabecula septomarginalis; *MPM = most anterior medial papillary muscle in medial papilla y complex.)

papillary muscles (AcPMs) are those that join the septal leaflet [17] (except for the part anterior to the membranous septum) at its free margin or rough zone. The highest one among them, often the most anterior, has been referred to as the uppermost accessory papillary muscle [15, 17 (uppermost AcPM). This muscle usually arises from the TSM and is located closely behind the medial papillary muscle [17]. The septal papillary muscles located between the lower margin of the membranous septum and the uppermost AcPM are referred to as the upper AcPMs and those below the uppermost, the lower AcPMs. These terms have been employed, merely on morphological criteria, in congenital cardiac anomalies as well. The identification of these muscles, however, is not infrequently equivocal because of deformity. Throughout this report, the word anterior has been employed to mean closest or toward the right ventricular outlet. Posterior indicates toward the right ventricular inlet, and underneath should be understood to mean deep on the left ventricular side of the ventricular septum, unless otherwise specified. Results The Table and Figures 2 and 3 present the data, histologically obtained in our specimens, on the topographical relationship of the conduction system to the adjacent structures that will be used throughout in the description of each type of cardiac anomaly. Features noted for each type will be summarized, and a comparative evaluation for each will be done from a surgical viewpoint.

Course of Atrioventricular Conduction System in Normal and Malformed Hearts NORMAL HEART. In 3 normal adult heart specimens, the compact AV node rested on the right fibrous trigone but was encompassed by the atrial septum. The penetrating bundle was a continuation of the AV node. After pene-

trating the right portion of the central fibrous body, the His bundle coursed beneath the membranous septum with a tendency to veer to the left ventricular side. The bifurcation lay astride the septum and proximal (within 2 mm) to the distal end of the membranous part. Across the septum at a shallow level, the RBB descended within the TSM beneath a series of upper AcPMs, including the uppermost one, and somewhat posterior to the MPM. On average, the RBB lay 0.1 mm anterior to the uppermost AcPM and 4 mm posterior to the MPM. The RBB therefore descended within the TSM toward the anterior papillary muscle through the moderator band, definitely anterior to the lower AcPMs, with a tendency to emerge gradually into the subendocardium. In an infant specimen, the tissues lay beneath a row of upper AcPMs possessing numerous chordae. Representative specimens of the normal adult and infant hearts are shown in Figure 4. ISOLATED VENTRICULAR SEPTAL DEFECT. Twelve pediatric heart specimens with isolated VSD were further classified [ 10, 131 as follows: perimembranous inlet (4), perimembranous trabecular (4),perimembranous infundibular (l),muscular infundibular (l),subarterial infundibular (l), and muscular inlet defect (1). The defects were extremely large in the majority of specimens. The course of the His bundle and the site of the bifurcation varied with the type of defect as well as the individual heart. In specimens with a perimembranous inlet defect, the His bundle ran superficially and astride the lower rim of the defect. In those with a perimembranous trabecular defect, it deviated on the left ventricular side of the rim. In the specimen with a perimembranous infundibular defect with aortic overriding, the His bundle distributed on the extreme left ventricular aspect of the rim. A similar course was noted in both the specimen with a muscular infundibular defect with mild aortic overriding and the specimen showing a subarterial infundibular defect. In each of the last 3 hearts, an excessive muscular mass was found on the right ventricular aspect. In specimens with perimembranous inlet or trabecular defect, the MPM arose from either the anterosuperior or the superior margin in the former and from the anterior in the latter, whereas the upper AcPMs arose from the septum caudal to the defect in both types of defect. The MPM predominantly stretched chordae to the medial portion of the anterior leaflet. The RBB passed almost beneath the upper AcPMs and uppermost AcPM in hearts with perimembranous inlet defect, and it passed beneath or slightly on the left ventricular side in those with perimembranous trabecular defect. However, it ran posteroinferior to the MPM at varying distances. The mean distance between the RBB and the uppermost AcPM was 0 mm in hearts with perimembranous inlet and 1.2 mm in those with trabecular defect; the mean distance between the RBB and the MPM was 5 and 2.5 mm, respectively. In all specimens with infundibular defect, whether the perimembranous, muscular, or subarterial type, the me-

601 Tamiya et al: Surgical Landmarks of the AV Conduction System

Topographical Relationship between the Right Bundle Branch and Papillary Muscle Tvcusp

of Aorta

MPM"

Position

Patient Disease

Dextro-

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Type of VSD

Age

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(DORV) "This means the cusp of the tricuspid valve that the MPM predominantly joins. bPatients 7 and 9 omitted because of deterioration of the structures; Patient 27 omitted because of an entirely different relationship due to a muscular trabecular type of defect in addition to deterioration. VSD = ventricular septal defect; TV = tricuspid valve; MPM = medial papillary muscle; uAcPM = uppermost accessory papillary muscle; NA = not applicable; ant. = anterior; post. = posterior; perim. = perimembranous; trab. = trabecular; inf. = infundibular; PM,, PM, = two papillary muscles; musc. = muscular; subart. = subarterial; ECD = endocardial cushion defect; CAVC(A) = complete atrioventricular canal Rastelli type A; TOF = tetralogy of Fallot; TI. Ar. AT, A4 = huncus arteriosus Van Praagh types 1 and 4; TGA = transposition of great arteries; I1 = type 11; DORV = doubleoutlet right ventricle; A = anterior; S = septal; C = commissure.

dial papillary complex rather atypically joined the tricuspid leaflet. In the specimen with perimembranous infundibular VSD and moderate aortic override (No. 13 in the Table), there were two papillary muscles: a small one (presumably the MPM) arising from the posterior wall of the defect and joining the commissure leaflet alone, and a large one arising from the TSM (presumably the uppermost AcPM), 6 mm below the defect (i.e., toward the apex), and joining the septal leaflet dominantly. The bifurcation lay underneath the small muscle, 3.5 mm deep (i.e., on the left ventricular side), and the RBB passed 3 mm anterior to the large one, 2 mm deep. In the specimen with muscular infundibular VSD and mild aortic override (No. 14), a poor MPM arose from

the midposterior wall of the defect with chordae joining the commissure leaflet alone. The His bundle ran 3.5 mm posterior to the MPM, and the bifurcation lay underneath the uppermost AcPM, 3 mm deep. In the specimen with subarterial infundibular VSD (No. 15), the MPM arose from the posterosuperior wall of the defect with chordae attaching to the commissure leaflet alone, and the His bundle passed 1 mm posterocaudal to the MPM, 3 mm deep, and the bifurcation lay 1 mm anterocaudal to it, 3 mm deep. The base of the uppermost AcPM could not be identified because of deterioration. Representative examples of perimembranous VSD are shown in Figure 5.

602 The Annals of Thoracic Surgery Vol 40 No 6 December 1985

TOP

I

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!.+ -

t-- 10mm

I I

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Fig 2 . Length of His bundle and topographical relationship between bifurcation (Bif.) and papillary muscles in our cardiac specimens. The length of the His bundle and the distance from the bifurcation to the uppermost accessoy papilla y muscle (uAcPM) or medial papillay muscle (MPM) were measured on the plane of the ventricular septum. The uppermost AcPM and the MPM marked on the baseline for each specimen do not mean their location on the right bundle (RB) branch, but merely indicate the distance from the bifurcation about the inlet-to-outlet direction of the right ventricle. (VSD = ventricular septal defect; NA = not applicable; BB = branching bundle; LBB = left bundle branch; PB = penetrating bundle; NBB = nonbranching bundle; perim. = perimembranous; trab. = trabecular; inf. = infundibular; musc. = muscular; subart. = subarterial; CAVC = complete atrioventricular canal; TOF = tetralogy of Fallot; Tr. Ar. A,, A., = truncus arteriosus, Van Praagh type A1 and A4; TGA = transposition of great arteries; I1 = type ZZ; DORV = double-outlet right ventricle.) COMMON ATRIOVENTRICULAR CANAL. In the specimen with complete AV canal (complete AV septal defect [9]), type A [18] (No. 17), no clear marks of the triangle of Koch were detected with the naked eye, presumably because of the combined lesion in the common atrium (Fig 6). Histologically, the AV node lay just to the right of the tendon of Todaro. The nonbranching portion of the His bundle traveled as far as 7 mm in the crest of the sinus septum just beneath the posterior common AV leaflet. The branching bundle ran on the left ventricular side of the crest of the lower rim of the VSD. The bifurcation lay in about the midportion of the lower rim and beneath the uppermost AcPM. The RBB curved down to the moderator band. The minimal distance between the

I

1

RBB and the MPM was 5 mm. Serial sections of the septum revealed that the branching bundle and the bifurcation lay beneath or cephalad (antiapical) to the base of the septal papillary muscles that joined the posterior AV leaflet. TETRALOGY OF FALLOT. Of 7 heart specimens with tetralogy of Fallot, 5 were classified as showing a perimembranous infundibular type of defect and 2 as showing a muscular infundibular type [lo]. All but 1 (No. 18) were pediatric specimens. Piercing the right portion of the central fibrous body, the His bundle deviated markedly to the left ventricular aspect of the defect, often obliquely across the crest of the lower rim where the membranous remnant attached. Histologically, such a shift of the bundle was roughly dependent on the hypertrophic posterior limb of the TSM.The bifurcation lay on the left ventricular aspect in the environs of the distal end of the membranous remnant, when the remnant was present, and usually near the left ventricular portion opposite the MPM. The branching portion ran more deeply than in normal hearts, particularly in those with the muscular infundibular type of tetralogy of Fallot. Traversing the anterior part of the posterior limb of the TSM somewhat deeply, the RBB usually descended in the body of the TSM somewhat anterior to the MPM; the RBB and MPM were about 2 mm apart on the average. The RBB did not enter the anterior limb around the lower rim of the defect in any of the specimens. The relationship of the RBB to the lower AcPMs remained normal.

603 Tamiya et al: Surgical Landmarks of the AV Conduction System

PB

NBB

BB

1 RBBl

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Fig 3 . (A) Left-to-right deviation of the conduction bundle in the ventricular septum at its running level in our specimens. ( B ) Distance from the lower rim of crest of defect to the conduction bundle. (PB = penetrating bundle; NBB = nonbranching bundle; BB = branching bundle; RBB = right bundle branch; SD = standard deviation; * = mean age except for adults; VSD = ventricular septal defect; perim. = perimembrunous; trab. = trabecular; inf. = infundibular; musc. inf. or MI = muscular infundibular; subart. inf. or SI = subarterial infundibular; TGA = transposition ofgreat arteries; It. vt. = left ventricle; rt. vt. = right ventricle; vt. sept. = ventricular septum; CAVC = complete atrioventricular canal; TOF = tetralogy of Fallot; Tr. Ar. = truncus arteriosus; Bif. = bifurcation; I1 = type 11; DORV = double-outlet right ventricle.) Patient 6 omitted because of extreme immaturity; Patient 27 omitted because of an entirely different relationship due to a muscular trabecular type of defect in addition of deterioration of the RBB.

The MPM originated in the posterior limb of the TSM, near the posterior lower rim of the defect in all but 1 adult heart (No. 18). In that specimen, it arose from the body of the TSM, 20 mm caudal to the lower rim. The MPM received chordae from the anterior leaflet in all but 1specimen (No. 24). In the exception, the MPM attached to both the anterior and septal leaflets. Representative specimens of tetralogy of Fallot of the perimembranous infundibular and muscular infundibular types are shown in Figure 7. TRUNCUS ARTERIOSUS. VSD in truncus arteriosus, Van Praagh type A1 and A4 [19], was a perimembranous subarterial defect in our specimens. In both hearts, the

nonbranching portion of the His bundle passed through the middle of the posterior rim, and the branching portion as well as the RBB ran with an anatomical relationship to the MPM such as seen in tetralogy of Fallot, namely, the RBB descended beneath or anterior to the MPM, which attached to the medial part of the anterior leaflet (Fig 8). TRANSPOSITION OF GREAT ARTERIES. In the specimen with TGA of a small apical VSD (No. 27), the penetrating and nonbranching bundle ran on the right ventricular side, and the branching bundle as well as the bifurcation lay along the midportion of the ventricular septum. The RBB was not traced because of deterioration. In the specimen with TGA type I1 [20] (No. 28), the nonbranching and the branching bundle took an extreme left ventricular course, with a tendency to gradually deepen toward the bifurcation (here, deep means approaching the left ventricular subendocardium). The RBB descended 2.5 mm anterior to the uppermost AcPM, 2 mm deep. The specimen with double-outlet right ventricle (DORV) (No. 29) had a perimembranous infundibular VSD under the pulmonary trunk (Fig 9). This heart was classified as TGA and not as a Taussig-Bing anomaly of the original type [21,22] because of the presence of continuity between the mitral and pulmonary valves. After penetrating the right portion of the central fibrous body, the His bundle descended in the septum, a few millimeters behind the posterior margin of the defect, with a gradual shift to the left ventricular subendocardium. The nonbranching and the branching portion measured 6.6

604 The Annals of Thoracic Surgery Vol 40 No 6 December 1985

Fig 4 . ( A ) Course of conduction system histologically confirmed in a 67-year-old m m a n with a normal heart (No. 2 in Table). ( B ) Course of conduction system histologically demonstrated in a normal heart of a 2-month-old boy (No. 4). (A-V = atrioventriculur; MPM = medial papillary muscle; RBB = right bundle branch; A, B = sites of photomicrographs; LV = left mtricle; RV = right ventricle; LBB = left bundle branch.

and 2 mm, respectively. There were two papillary muscles, which should belong to the medial capillary complex: the upper, smaller one attached to the commissure leaflet and the lower, larger one, the MPM, attached mainly to the anterior leaflet. The His bundle descended behind both papillary muscles. The bifurcation lay 4 mm posteroinferior to the MPM, 5 mm deep, and the RBB swept down the uppermost AcPM anteriorly, toward the anterior papillary muscle. Comparison of Course of Conduction System and Surgical Landmarks among Cardiac Anomalies LENGTH OF HIS BUNDLE,

A N D RELATIONSHIP BETWEEN

The total length of the ventricular His bundle, namely, the nonbranching plus the branching portion, was within 7 mm in most of our pediatric specimens, except for complete AV septa1 defect and DORV type of TGA (see Fig 2). The bifurcation lay posterior to both the MPM and uppermost AcPM in normal hearts. This feature was retained in both perimembranous inlet and trabecular VSDs in principle. The bifurcation usually lay close to the MPM alBIFURCATION AND PAPILLARY MUSCLES.

B

605 Tamiya et al: Surgical Landmarks of the AV Conduction System

A

B Fig 5. (A) Course of conduction system in a 6-six-month-old boy who underwent corrective operation for wntriculur septal defect (VSD) (No. 5). The defect is perimembranous inlet type. Two papillary muscles arise from the psteroinferior rim of the defect, i.e., the upper and uppermost accessory papillary muscle (uAcPM). The His bundle and bifurcation shallowly lie beneath these muscles, although distorted by suturing. ( B ) Course of conduction system in a 6-month-old boy with VSD of perimembranous trubeculur type (No. 10) (PplPs = 93%).

(C)Course of conduction system in a 7-month-old girl with VSD of perimembranous infundibular type (No. 13) (PplPs = 100%). Presumably the PM1 would be the medial papillary muscle (MPM) and the PM2,the uppermost AcPM. (RBB = right bundle branch; A-V = atrioventricular; A, B = sites of photomicrographs;LBB = 1t$ bundle branch; LV = left ventricle; RV = right ventricle; PplPs = systolic pulmonary pressurelsystolic systemic pressure.)

Fig 6 . Course of conduction system in a 13-month-old boy with complete atrioventricular (A-V) canal, type A, and common atrium (No. 17). Note the nonbranching bundle asfride the crest of the ventricular septum, and the branching bundle and bifurcation lying on the left 606

ventricular aspect, cephalad to the base of accessory papillary muscles (PM).(A, B, C = sites of photomicrographs;M P M = medial papill a y muscle; LV = left ventricle; RV = right ventricle.)

Fig 7. (A) Course of conduction system in a 1-year-old girl with tetralogy of Fallot (TOF) of perimembranous infundibular type defect (No. 19). The right bundle branch (RBB)is found 3 mm anterior to the medial papillary muscle (MPM) and 2 mm deep. The RBB still sweeps down the MPM anteriorly, demonstrating that the MPM should be the fibrous structure shaping the anterior margin of the membranous flap. (B)Course of conduction system in an 8-month-old girl with tetralogy of Fallot of muscular infundibular type defect (No. 607

23). From the left to the right ventricular side, the distal His bundle and the proximal RBB ride obliquely across a firm muscle bar which constructs the posterior and inferior rim of the defect, and descend in the trabecula septomarginalis (TSM). The RBB lies 4 mm anterior to the MPM and about 0.5 mm deep. (A-V = atrioventricular; A, B, C = sites of photomicrographs; LV = left ventricle; TV = tricuspid value; RA = right atrium; RV = right ventricle.)

608 The Annals of Thoracic Surgery VoI 40 No 6 December 1985

Fig 8 . Course of conduction system in a 2-month-old boy with truncus arteriosus, type A1 (No. 25). The defect is of perimembranous subarterial type. The right bundle branch (RBB) passes beneath fhe medial papillary muscle (MPM). (A-V = atrioventricular; A, B = sites of insets; LV = left ventricle; TV = tricuspid valve; RV = right ventricle.)

though on the opposite ventricular side in perimembranous infundibular VSD, tetralogy of Fallot, and truncus arteriosus. COURSE OF SPECIALIZED ATRIOVENTRICULAR CONDUCTION BUNDLE. Figure 3 is a stereographic illustration of

the course of the conduction bundle, namely, the axis in the ventricular septum. Figure 3A shows the left-to-right deviation of the course at the running level of each portion of the bundle, and Figure 38 indicates the distance from the crest of the lower rim of the defect to each portion of the bundle, that is, the depth toward the apex. The measured site of the His bundle was at about the midpoint of the penetrating, nonbranching, and branching portions and the bifurcation. That of the RBB was at the base of the uppermost AcPM in principle, although the MPM was used instead of the uppermost AcPM in tetralogy of Fallot and truncus arteriosus for a reason to be mentioned in the comment. In general, the width of the ventricular septum at the running level of the His bundle was substantially narrower in infants than in adults. It was particularly striking in the posteroinferior rim of the perimembranous infundibular defect in infants with tetralogy of Fallot or truncus arteriosus.

In perimembranous inlet VSD and complete AV septal defect, the His bundle superficially ran astride the summit of the septum. The bundle in perimembranous trabecular VSD ran slightly more to the left ventricular side and more deeply than in the inlet type. That in perimembranous infundibular VSD ran more to the left ventricular side and more deeply than in the trabecular type. The deviation from the lower rim was further increased in muscular infundibular VSD. The His bundle in tetralogy of Fallot of the perimembranous or muscular defect type showed a tendency of course similar to VSD of each type. It ran relatively shallowly on the posteroinferior rim in the perimembranous defect type and deeply in the muscular defect type. The His bundle in truncus arteriosus descended obliquely along and near the midportion of the thin posteroinferior wall of the defect. The bundle in TGA took an extremely left ventricular course, as far as the 2 specimens with perimembranous defect were concerned. RELATIONSHIP BETWEEN COURSE OF CONDUCTION BUN-

The Table indicates the portion of the tricuspid valve where the MPM (or the medial papillary complex) dominantly attached, as well as the relationship between the conduction bundle and papillary muscles. The dominantly attached portion appeared to be inherent to each type of defect. It was the anterior leaflet in perimembranous inlet or trabecular VSD, and the commissure leaflet or the anterior plus the septal leaflet in infundibular VSD. It was the anterior leaflet in both tetralogy of Fallot and truncus arteriosus. The topographical relationship in normal hearts, in DLE AND PAPILLARY MUSCLES.

609 Tamiya et al: Surgical Landmarks of the AV Conduction System

Fig 9 . Course of conduction system in a 2-month-old boy with transposition of great arteries (TGA) of double-outlet right ventricle (DORV) type (No. 29). The defect is of perimembranous infundibular type. (A-V = atrioventricular; A, B = sites of photomicrographs; MPM = medial papillary muscle; RBB = right bundle branch; Ant. PM = anterior papillary muscle; VSD = ventricular septa1 defect; TV = tricuspid valve; RV = right ventricle.)

which the RBB ran beneath or slightly anterior to upper AcPMs and most usually posterior or inferior to the MPM, was conserved in hearts with perimembranous inlet or trabecular VSD. The RBB usually ran anterior to the MPM in hearts with tetralogy of Fallot or truncus arteriosus. Such a tendency also was noted in hearts with infundibular VSD.

Summary Figure 10 is a diagram summarizing the perimembranous defects. It shows the topographical relationship of the conduction tissues to the neighboring structures. In isolated perimembranous inlet or trabecular VSD, the bifurcation and the RBB lay about beneath a series of upper AcPMs, when these tension apparatuses were present. The RBB descended beneath or slightly anterior to the uppermost AcPM and posteroinferior to the MPM. This relationship was basically the same as in the normal heart. In tetralogy of Fallot, the bifurcation usually lay underneath the MPM, on the left ventricular side of the septum. Traversing the septum, the RBB descended slightly anterior to the MPM. In isolated infundibular VSD, the relationship between the bifurcation

and the RBB with the adjacent papillary muscles was intermediate between both diseases just mentioned, and seemed modified by the grade of aortic overriding. Aspects of the TSM such as distribution and hypertrophy appeared to be important factors in further modifymg the relationship between the course of the conduction bundle and the adjacent papillary muscle.

Comment Some surgically induced conduction disturbances lead to grave complicationsin both the early [1,2,23] and late [3, 241 postoperative periods. Extensive clinical and research work has provided guidelines to prevent these complications, but many problems remain unsolved. Precise topographical knowledge is essential to obtain the solutions. The topography of the conduction system, particularly that of the His bundle, in congenital malformation of the heart has been well documented. Histological studies by Lev [4-61 offer us a classic text, and recent studies by Anderson and colleagues (7-101 are particularly worthwhile for surgical anatomy. Our histological observations in this respect were generally the same as those they reported. No elaborate discussion is required. It remains for us only to add some information that we deem of help for surgical repair. A precise description of the intracardiac structure is desirable for cardiac surgeons to establish clear anatomical landmarks of the conduction system. With respect to the medial papillary complex, for example, Wenink [15] pointed out the difficulty of standardizing the nomencla-

610 The Annals of Thoracic Surgery Vol 40 No 6 December 1985

(normal heart)

1 ) perim. inlet VSD

Pm

lower AcPMs’

2) perim. trabecular VSD

AcPM

3) TOF

(perirn. infundibular VSD type)

MPM

Fig 10. Topographical relationship between the specialized conduction system and adjacent structures, with special reference to the papillary muscles of the right wntricle. (Memb. = membranous; A-V = atrioventricular; MPM = medial papillary muscle; AcPM = accessory papillary muscle; TSM = trabecula septomarginalis; RBB = right bundle branch; perim. = perimembranous; VSD = ventricular septal defect; bif. = bifurcation; TOF = tetralogy of Fallot.)

ture. His suggestion [15] is quite comprehensible, because of the individual and age-dependent morphological varieties and indistinct boundaries of the medial papillary complex. The anatomical terms arbitrarily designated by us here are used only for convenience to describe their anatomical relationship with conduction tissues as precisely as possible. The major danger area for AV block has been said to be the confluence of the aortic, tricuspid, and mitral valves shaping the posteroinferior wall of the perimembranous defect [B]. We [23, 241 initially encountered a high incidence of AV block in infants with isolated perimembranous inlet VSD or tetralogy of Fallot with perimembranous infundibular defect. The superficial run of the His bundle astride the lower rim of the defect, which we suggested with electrophysiological studies (251 and confirmed histologically, should be an important causative feature in the former condition. The unusually close relationship between the penetrating bundle and the base of the free septal leaflet should be a critical factor in the latter. Our data support the belief of Anderson and colleagues [8] that the free leaflet pf the tricuspid valve is the optimal structure for the placement of sutures in the posteroinferior wall of the defect; no conduction tissues were encased by the tricuspid valve in our specimens either. It has been well documented that the branching bundle most usually distributes on the left ventricular aspect of the septum in tetralogy of Fallot [4, 6, 8, 261. An abnormally located hypertropic

posterior limb of the TSM should be the main cause of this distribution [ 2 7 . The MPM, when present, may often serve as a gross surgical landmark for bifurcation and the first part [6] of the RBB in this anomaly, since the His bundle bifurcation was on the left ventricular aspect opposite the MPM and the RBB descended slightly anterior to it in most of our specimens with tetralogy of Fallot. Surgically induced right bundle-branch block has become one of our current interests [28]. There have been relatively few reports on the topographical relationship of the RBB with the papillary muscles of the right ventricle (4, 5, 291. Becu and co-workers [30] pointed out that the medial papillary complex showed a variable relationship to perimembranous defects. However, they did not give a detailed account of the relationship between the RBB and the adjacent papillary muscles. Our observations in this matter are as follows. In perimembranous VSD without aortic override such as defects of the inlet or trabecular type, the RBB definitely had a closer relationship to the upper AcPMs than to the MPM, as is the case in the normal heart. However, in perimembranous VSD with aortic override such as tetralogy of Fallot, the RBB showed a closer relationship with the MPM. Okada 131,321 is of the opinion that there should be a certain relationship between the RBB and the “muscle of Lancisi” on the basis of his definition of this muscle.* According to his work in embryology, the RBB develops along the tricuspid ledge; therefore, there is an intimate relationship between the conduction tissues and the papillary muscles that develop from the ledge. “The tricuspid ledge” described by Spitzer 133) is the primordium of the tension apparatus for the tricuspid valve. The muscle of Lancisi designated by Spitzer [33] is a part of the tricuspid ledge, presumably of primitive ventricu‘Okada R Personal communication, 1979.

611 Tamiya et al: Surgical Landmarks of the AV Conduction System

lar origin, and therefore should differ from the medial papillary muscle as commonly defined at present. Okada’s “muscle of Lancisi,” in our opinion, could be better regarded as the uppermost AcPM. Van Mierop and his group (34-361 documented maldevelopment of the septum of the conus on the basis of their embryological studies of keeshond dogs and other investigations. They believed that hypoplasia of the conus septum should be the essential lesion responsible not only for the persistence of a large interventricular communication with dextroposition of the aorta, but also for the absence of the medial papillary muscle and abnormality of the medial portion of the anterior tricuspid leaflet. Van Mierop [17] pointed out that the uppermost AcPM has often been mistakenly interpreted to be the medial papillary muscle in such a malformation. If the assumption of these researchers is valid, the papillary muscle described here as the MPM, merely on morphological grounds in tetralogy of Fallot and truncus arteriosus, should be, embryologically speaking, the uppermost AcPM. This point of view simplifies the topographical relationship that we observed between the RBB and the adjacent papillary muscle in most cardiac anomalies. In other words, the RBB always runs beneath or anterior to the embryological uppermost AcPM, regardless of the type of defect. The relationship between the RBB and upper AcPMs appeared to be more or less modified by the attitude of the TSM intervening there, a finding in the work of Kurosawa and Becker [27] and in our studies. The developmental process of the AV conduction tissues described by Anderson and associates [37] may be summarized as follows. Around horizon 15, the tissues are demonstrable prior to fusion of the endocardial cushions. The bundle astride the posterior septum becomes directly continuous with a sheet of cells draped across the bulboventricular part of the interventricular septum. This bundle, an invagination of the AV ring tissues [ l l , 121, forms the primordium of the compact node, and the sheet, assumed to be the bulboventricular ring tissues (11, 121, forms the primordium of the bifurcating bundle. This arrangement of the conduction tissues prior to fusion of the endocardial cushion is reflected in the disposition observed in endocardial cushion defects of the complete type. The latter tissues are observed on the TSM at an early stage when the primary interventricular foramen is yet patent. Goor and Lillehei [38] introduced another developmental mechanism of the tricuspid valve. A spur of the right lower tubercle of the posterior AV cushion spreads over the right surface of the sinus septum during horizons 17 and 18. The undermining process between the spur and the sinus septum progressively splits a septal leaflet off the sinus septum, and the septum becomes trabeculated during horizons 21 and 22. The tension apparatus of the septal leaflet is molded by this undermining process. On the other hand, the right lateral AV cushion and the end of the conus ridge 3 (presumably identical to the right bulbar ridge) are the main mesen-

chymal tissue suppliers in primordial formation of the anterior leaflet. Van Mierop (171 wrote that the lowermost portion of the conus septum becomes the most medial portion of the anterior leaflet, its corresponding chordae tendineae, and the medial papillary muscle through the undermining process. The medial papillary complex designated by Wenink (151 seems to involve a wider scope than ours. He suggested that it originates from the left and right bulbar ridges, AV cushion, and myocardium. He stressed that the undermining of the right bulbar ridge can produce trabeculation or even chordae at the site where the crista supraventricularis and the anterior leaflet meet. In his fetal observations [ll], the upper part of the bulboventricular ring, which was close to the right bulbar ridge, did not contribute to the definitive conduction system, whereas the left and ventral part of this ring, which had an intimate relationship with the left bulbar ridge, continued in a dorsocaudal position astride the muscular ventricular septum and ran into the AV ring. In the definitive heart, the topographical relationship of some papillary muscles to conduction tissues is surprisingly intimate. We [25] initially noticed this during intraoperative electrophysiological delineation of the tissues. Fibrous connections between the RBB and the adjacent papillary muscles were a common finding in our specimens; however, the intimacy varied with the individual muscle. For example, the medial papillary muscle had less intimacy with the RBB than did a series of upper AcPMs. Provided that the undermining for primordial formation of upper AcPMs is limited to the upper inflow portion of the right ventricle and that the process of the medial papillary muscle is limited to the infundibular portion, the bulboventricular transition where the RBB develops should shape a rough boundary for both undermining territories. Judging from the embryology of the tricuspid valve proposed by Goor and Lillehei [38] and the ring tissue theory of Wenink [ll, 121, there should be a closer intimacy of the conduction tissues with the upper AcPMs than the MPM in the normal heart. Should interventricular foramen be left unclosed, the MPM would lose or reduce the chance of gaining access to the ventricular septum where the bifurcating bundle is disposed, as observed in perimembranous inlet defect and complete AV septal defect. In serial sections of the ventricular septum, the bifurcation of the His bundle usually lay underneath or cephalad (antiapical) to the base of upper AcPMs or chordae. It was also occasionally observed in the branching portion. Similarly, the RBB rarely ran on the right ventricular inflow side of the base of these tension apparatuses. Wenink (11, 121 hypothesized that the common bundle and the RBB in the TSM are remnants of the bulboventricular ring. The embryology of Goor and Lillehei (381 and of Van Mierop may support such topographical relations as we observed. These findings have provided us rough but still practical guidelines for suture placement. AV conduction disturbance, including

612 The Annals of Thoracic Surgery Vol 40 No 6 December 1985

bilateral bundle-branch block, has not been encountered and complete right bundle-branch block has decreased to less than 30% in the past three years, that is, since such histological information began to be used clinically. Recently we have begun to employ an electronic computer system for better spatial recognition of the conduction system.

Addendum Recently, we examined a cardiac specimen of perimembranous trabecular VSD in which the medial papillary muscle received chordae tendineae, attaching not only to the anterior leaflet of the tricuspid valve, but also to the septal leaflet as do the upper AcPMs. This muscle was located at the lower rim of the defect as presented by Soto and co-workers [13], and the RBB ran beneath the muscle. lt may be interpreted to support the affinity of the RBB with the component of upper AcPMs. Supported in part by Grant-in-Aid for Scientific Research No. 8-58480293 from the Ministry of Education, Science, and Culture, Japan. We express our sincere gratitude to Dr. Ryozo Okada, Professor of Internal Medicine, Juntendo University, Tokyo, and Dr. Hiromi Kurosawa, Instructor at the Cardiovascular Center, Tokyo Women’s Medical College, Tokyo, for their instruction in cardiac anatomy, embryology, and histology. We also acknowledge our deepest indebtedness to the following institutes and individuals for kindly offering valuable cardiac specimens: Cardio-Pulmonary Center, Tsurumai Prefectural Hospital, Chiba (Dr. Tsunetaro Nakamura, Chief); Fukui Cardiovascular Center, Fukui (Dr. Takashi Tanaka, President); Cardiovascular Center, Amagasaki Prefectural Hospital, Amagasaki (Dr. Yoshio Yokota, Chief); the Second Pediatric Division, National Okayama Hospital, Okayama (Dr.Kazuma Tateishi, Chief); and the First and Second Departments of Pathology, Kurume University, Kurume (Dr.Toshiro Nakajima and Dr. Teruyuki Nakajima, professor in each department). We are very grateful to Mr. Conrad Zagory, Jr., lecturer, and Miss Hiroko Morita at Kochi Medical School, and Miss Eva Garcia del Saz for their devoted cooperation in this work.

References 1. Lauer RM, Ongley PA, DuShane JW, et al: Heart block after repair of ventricular septal defect in children. Circulation 22526, 1960 2. Rosenbaum MB, Corrand G, Oliveri R, et al: Right bundle branch block with left anterior hemiblock surgically induced in tetralogy of Fallot. Am J Cardiol2612, 1970 3. Godman MJ, Roberts NK, Izukawa T Late postoperative conduction disturbances after repair of ventricular septal defect and tetralogy of Fallot: analysis by His bundle recordings. Circulation 49:211, 1974 4. Lev M: The architecture of the conduction system in congenital heart disease: 11. Tetralogy of Fallot. Arch Pathol 67:572, 1959 5. Lev M: The architecture of the conduction system in congenital heart disease: 111. Ventricular septal defect. Arch Pathol70529, 1960 6. Lev M: The conduction system. In Gould SE (ed): Pathology of the Heart and Blood Vessels. Third edition. Springfield, IL, Thomas, 1968, pp 180-220 7. Milo S, Ho SY, Wdkinson JL, Anderson RH: Surgical anatomy and atrioventricular conduction tissues of hearts

with isolated ventricular septal defects. J Thorac Cardiovasc Surg 79:244, 1980 8. Anderson RH, Allwork SP, Ho SY, et al: Surgical anatomy of tetralogy of Fallot. J Thorac Cardiovasc Surg 81:887, 1981 9. Thiene G. Wenink ACG, Frescura C, et al: Surgical anatomy and pathology of the conduction tissues in atrioventricular defects. J Thorac Cardiovasc Surg 82928, 1981 10. Anderson RH, Becker AE: Surgical anatomy. In Stark J, de Leva1 M (eds): Surgery for Congenital Heart Defects. New York, Grune & Stratton, 1983, pp 11-34 11. Wenink ACG: Development of the human cardiac conduction system. J Anat 121:617, 1976 12. Wenink ACG: Embryology of the conduction system. In Van Mierop LHS (ed): Embryology of the Heart and the Great Arteries. Leiden, Leiden University Press, 1978, pp 3-14 13. Soto B, Becker AE, Moulaert AJ, et a1 Classification of ventricular septal defects. Br Heart J 43:332, 1980 14. Anderson RH, Becker AE: Cardiac Anatomy. London, Gower Medical, 1980 15. Wenink ACG: The medial papillary complex. Br Heart J 39:1012, 1977 16. Silver MD, Lam JHC, Ranganthan N, et al: Morphology of the human tricuspid valve. Circulation 43:333, 1971 17. Van Mierop LHS: Anatomy and embryology of the right ventricle. In Edwards JE, Lev M, Abell MR (eds): The Heart. Baltimore, Williams & Wilkins, 1974, pp 1-16 18. Rastelli GC, Kirklin JW, Titus JL: Anatomic observations on complete form of persistent common atrioventricular canal with special reference to atrioventricular valves. Mayo Clin Proc 41:2%, 1966 19. Van Praagh R, Van Praagh S: The anatomy of common aorticopulmonary trunk and its embryologic implications: a study of 57 necropsy cases. Am J Cardiol 16:406, 1965 20. Mustard WT: Recent experience with surgical management of transposition of great arteries. J Cardiovasc Surg (Torino) 9:532, 1968 21. Taussig HB, Bing RJ: Complete transposition of the aorta and a levoposition of the pulmonary artery: clinical, physiological, and pathological findings. Am Heart J 37551, 1949 22. Van Praagh R What is the Taussig malformation? Circulation 38445,1968 23. Tamiya T. Liao YN, Namikawa M Atrioventricular block induced in open-heart surgery. Geka 35:1222, 1973 24. Tamiya T, Yamashrio T: Analytical studies of the conduction disturbance surgically induced in congenital heart disease. Kyobu Geka 35:918, 1982 25. Tamiya T, Yamashiro T, Kitagawa S, et al: Electrophysiological delineation of the specialized conduction system during cardiotomy and its clinical application. Int Surg 68:107, 1983 26. Hasegawa T Studies on the conduction system in congenital malformation of the heart, especially of tetralogy of Fallot. Jpn Heart J 2:377, 1961 27. Kurosawa H, Becker AE: Modification of the precise relationship of the atrioventricular conduction bundle to margins of the ventricular septal defects by the trabecula septomarginalis. J Thorac Cardiovasc Surg 87604, 1984 28. Tamiya T, Yamashiro T, Nishizawa T, et al: Surgical right bundle branch block. Kyobu Geka 34:165, 1981 29. Kurosawa H, Becker AE: Surgical anatomy for the right bundle branch block. Kyobu Geka 35:179, 1982 30. Becu LM, Fontana RS, DuShane JW, et al: Anatomic and pathologic studies in ventricular septal defect. Circulation 1 4 9 9 , 1956

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31. Okada R Embryological consideration of cardiac anomalies (2). Kokyu To Junkan 21547, 1973 32. Okada R The conduction system of the heart: its anatomy,

embryology and pathology related to congenital malformation. Shoni Geka 121310, 1980 33. Lev M, Vass A, translators: Spitzer's Architecture of Normal and Malformed Hearts: A Phylogenic Theory of Their Development. Springfield, lL, Thomas, 1951, pp 49-55 34. Van Mierop LHS, Patterson DF, Schnarr WR: Hereditary

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development of the cardiac specialized tissue. In Wellens HJJ, Lie KI, Janse MJ (eds): The Conduction System of the Heart. Leiden, Stenfert Kroese, 1976, pp 3-28 38. Goor DA, Lillehei CW: The embryology of the heart: I. The heart and its systemic tributaries. In Goor DA, Lillehei CW (eds): Congenital Malformations of the Heart. New York, Grune & Stratton, 1975, pp 38-88

REVIEW OF RECENT BOOKS Management of Vascular Trauma Edited by Morris D . Kernstein, M . D . Baltimore, University Park Press, 1984 224 pp, illustrated, $32.00

to the vascular fellow, the practicing vascular surgeon, and the trauma surgeon involved in management of vascular trauma.

Reviewed by Steven R . Shackford, M . D .

Atlas of Surgical Anatomy for General Surgeons Steven W . Gray and john E . Skandalakis Baltimore, Williams 6 Wilkins, 1985 361 pp, illustrated, $148.00

This concise text is an important contribution to both the trauma literature and the literature in vascular surgery. Management of Vascular Trauma is well organized and well written. The chapter authors have combined current references and extensive review of the literature with their own experience in dealing with the subjects they cover. The introductory chapter on the biomechanics of vessel injury and wound ballistics is especially succinct and clear. Chapters on vascular injuries of the neck, thorax, and abdomen address and provide detailed discussion of controversies in the management of these injuries. There are also chapters on more general topics, such as fasciotomy, and on the use of antibiotics in vascular trauma. A chapter on vascular injury associated with drug abuse is excellent and long overdue. The chapter on microvascular surgery in trauma is well done, but too extensive and detailed for the proposed readership. The book concludes with a chapter on the use of synthetic prostheses in vascular trauma, a timely topic of major concern to all surgeons who deal with vascular trauma. The volume emphasizes problems commonly encountered in civilian vascular trauma, and it should be considered as a supplement to Rich and Spencer's fine text on military vascular trauma. Whereas Rich and Spencer take a broad approach to the subject, the editor of Management of Vascular Trauma focuses more on surgical judgment than on anatomy and surgical technique. Therefore, this book is intended for and recommended

San Diego, CA

Reviewed by Richard M. Peters, M . D .

This book is introduced with a statement about the progressive confinement of general surgery. The volume should prove useful to thoracic as well as general surgeons because it provides thorough coverage of regions of anatomy that may concern either surgical discipline. The illustrations, which present both common and variant anatomy, are well done. My review concentrated on the neck, esophagus, diaphragm, stomach, and colon. Each section starts with embryology and then moves on to congenital defects. The illustrations focus on features of anatomy and anatomical variants of most concern to surgeons. The book is not an operative manual but rather, as its title states, an atlas of surgical anatomy. This volume should be beneficial to the learning surgeon at all stages and will provide a helpful reference for reviewing such outreaches of anatomy as tracheal repair, substemal goiter, crural anatomy, diaphragmatic incisions, and variants of the inferior phrenic vessels. Surgeons interested in general thoracic surgery should find the book useful, and directors of training programs should consider it of value to their preceptees. San Diego, CA