.. ..- . o ' — A‘A‘ ‘M-‘JM-“A“A - ' ..‘ ‘ - ‘ o . . c . THE EXTENT OF CARDIAC MUSCLE IN THE GREAT VESSELS OF THE DOG T‘Iusls Ior II" Dag?" OI M, S. MICHIGAN STATE UNIVERSITY Rexford E. Carr-ow 19-60 THESIS LIBRARY Michigan State University THE EXTENT OF CARDIAC MUSCLE IN THE GREAT VESSELS OF THE DOG By REXFORD E CARROW A THESIS Submitted to the College of Veterinary Medicine Michigan State University of Agriculture and Applied Science in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE Department of Anatomy 1960 ii Frontispiece The gross structure of a canine heart showing the extent of cardiac muscle in the great vessels. 111 mHommm> 3350 95 ”7303 mmobU mo mogownh 350:0an .m \ m>m0 Hmonm mdmmgnHOmm mpno< iv TABLE OF CONTENTS Page INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . 1 Chapter 1. REVIEW OF LITERATURE . . . . . . . . . . . . . . . . 2 Superior Vena Cave and Azygos Vein 2 Inferior Vena Cava 5 Pulmonary Veins 6 Pulmonary Artery and Aorta 7 II. MATERIALS AND METHODS . . . . . . . . . . . . . . . . 9 III. RESULTS AND DISCUSSION . . . . . . . . . . . . . . . 10 Superior Vena Cava lO Azygos Vein 11 Inferior Vena Cava 12 Pulmonary Veins 13 Pulmonary Artery and Aorta _ 14 IV. smarmooncwsmus'............... 15 LITERATURE CITED . . . . . . . . . . . . . . . . . . . . . . . 17 ACKNOWLEDGMENTS The author wishes to express his sincere appreciation to Dr. M. Lois Calhoun, Head, Department of Anatomy for her encouragement, guidance and inspiration as a teacher that this investigation might be completed. The writer wishes to thank Dr. Charles Titkemeyer whose suggestions and collection of materials were helpful in the completion of this study. The author is also grateful to Esther M. Colby for her assistance in the technical laboratory, and to James Tucker for his help in the preparation of the photomicrographs. Thanks are also extended to Drs. Madan Bharadwaj, Thomas Bell and Esther Smith for their assistance in organizing the manuscript. Special thanks to the authors' wife for her encouragement and patience through the period of this study. vi LIST OF TABLES Table Page I Cardiac muscle measurements in the great veins. . . . . . 16 Plate II. III. IV. VI. VII. VIII. IX. XI. XII. XIII. XIV. XV. XVI. XVII. LIST OF PLATES Superior vena cava near heart showing cardiac muscle Arrangement of cardiac muscle in superior vena cava Termination of cardiac muscle in superior vena cava Fibrous attachment to cardiac muscle in superior vena cava Junction of azygos vein and superior vena cava Arrangement of cardiac fibers in azygos vein Termination of cardiac muscle in azygos vein Termination of cardiac muscle in inferior vena cava Inferior vena cava near heart showing cardiac muscle Inferior vena cava showing one of the vasa vasorum Fibrous attachment to cardiac muscle in the inferior vena cava Cardiac muscle in the pulmonary vein Pulmonary vein near heart showing arrangement of cardiac muscle Arrangement of cardiac muscle fibers of pulmonary vein in cross section Fibrous attachment to cardiac muscle in pulmonary vein Junction of pulmonary artery and heart Junction of aorta and heart vii Page 20 20 22 22 24 24 26 26 28 28 30 30 32 32 34 34 36 INTRODUCTION Although scientific literature contains innumerable reports of investigations on various parts of the circulatory system, none has been found which gives a histological picture of the extent of cardiac tissue in the great vessels of the heart. There are many references to the muscular content of the superior vena cava and a few gross studies which describe the muscle arrangement in the inferior vena cava and pulmonary vein. This investigation is an attempt to correlate the data already written on the muscular content of the vessels surrounding the heart and to determine how far cardiac muscle extends into the superior and inferior vena cava, pulmonary vessels, and aorta from the musculature of the heart. This study is confined to the dog. REVIEW OF LITERATURE Superior Vena Cava and Azyggs Vein A great many investigators have mentioned that cardiac muscle exists for some distance in the great vessels around the heart. Often these reports have been made in connection with work on the sino-atrial node. Muir (1955), remarked that nodal fibers in the rat are continuous with the inner circular and outer longitudinal cardiac muscle fibers Of the vena cava. Shaner (1929), contended that the S-A node anlage is in the muscular wall of the superior vena cava in cattle, but failed to mention the type of mmscle. Meyling and ter Borg (1957), and Truex and Copenhaver (1947), reported that fibers of the conduction system are connected with the ordinary heart muscle of the sinus venosus, and that the transition from nodal to cardiac type fibers is gradual. Flack (1910), not only found this to be true but added that in the mammalian heart there are possibly other fascicles of cardiac muscle around the orifices of the pulmonary veins. A histological study of the S-A region by Davies and Blair (1935), confirmed the continuity of muscle fibers in the sino-auricular region with those of the coronary sinus and atrium in bovine and man. The extent and type of muscle fibers found were not determined. According to Davies and Blair, three investigators in the mid-twenties, Brune, Pace, and Segre, working with ruminants and man, found that there is no connection between fibers of the S-A node and the muscle of adjacent vessels. The type and extent of the muscle in these vessels were not mentioned. 3 Keith and Flack (1907), issued a comprehensive report on the muscular connections between the divisions of the heart in mammals, using sixteen different vertebrate animals from several classes of the phylogenetic series. The authors reported that the higher an animal is in the vertebrate scale, the less the amount 6f sinus muscle present. Unlikeymany references on studies of this nature, Keith and Flack stated that there is a layer of longitudinal heart muscle fibers which passes uninterrupted from the auricular septum into the superior vena cava. In the porpoise, the musculature of the pre-cava is largely of the primitive type, while in the dolphin and ram there is no difference between the musculature of the superior vena cava and auricle. Nomura (1952), working only with the mouse, remarked that the muscular components of the nodal systemflrarely exhibit direct continuity with ordinary heart muscle. The anatomy of the valvular mechanisms around the venous orifices of the heart has been investigated frequently. Keith (1903), analysed these structures in mammalian and reptilian embryos and found that "loop-shaped cardiac muscle fibers" surround the terminal one-half inch of the superior vena cava. This is the earliest report which includes measurements of the extent of cardiac muscle in any vessels. Several gross studies on the heart, and structures adjacent to it, have been reported and these supply us with some useful and interesting information. Papez (1920), described the musculature of the atria in man, cattle and dog. He observed that the main bundles of muscles of the atria spread in all directions from their origins around the opening of the superior vena cava. Many of the superficial bundles begin in the region of the S-A node. These extend in a circular pattern up the caval wall. Glomset and Glomset (1940), confirmed these results, but Muir (1955), noted that the superficial layers of cardiac muscle in the wall of the superior vena cava of the rat are not circular but longitudinal. Papez (1920), reported that in man, beef and dog all muscle above the S-A node is in the superior vena cava and in dog the cardiac muscle is as far as and surrounds the beginning of the azygos vein. The.muscle in the caval iwall extends away from the heart for two or more centimeters. Glomset and Glomset (1940), found this distance to be from one-half to two inches depending on the species of domestic animal. Luschka (1863), and Robb (1934), recognized that cardiac tissue continues for a brief distance from the atria onto the wall of the great veins. Thomas (1959), completed a study on the pig and dog with results comparable to those of PapeZ' (1920). Both investigators found two definite layers of cardiac muscle at the terminations of the Venae cavae. They found that cardiac muscle extends along the pre-cava onto the last tributary of that vessel, the azygos vein, but neither investigator made any measurements. It was also found that heart muscle ends by dwindling out in the venae cavae and azygos vein. Thomas added that there are no major differences in the muscular arrangements of the venae cavae in the pig and dog. However, he mentioned that in the dog cardiac muscle extends from the superior vena cava into the azygos vein while in the hog this never occurs. Arey (1957), Krolling and Grau (1960), stated that cardiac muscle extends into the adventitia of the vena cava, but the exact distance was not given. Anatomists and physiologists have written much concerning the structure of the heart. Numerous articles have been written on the origin and conduction of the motor impulses of the heart. Maximow and Bloom (1957), reported that the impulse arises in the sinus venosus. Since most investigators are in agreement that it is cardiac muscle which tranmits the impulse, 5 it is obvious that heart tissue must be present in the sinus. In a comprehensive physiological study, Lewis, ££_§l, (1914), working entirely with dogs, found that conducting impulses are conveyed by cardiac muscle. These impulses cease at the termination of heart muscle in the venae cavae. Using electrical probes placed at various points on the walls of the superior and inferior vena cava they discovered that the excitatory process spreads cranially in the cardiac muscle of the vena cava. Some research workers have said that the conduction time in the superior vena cava is slow. However, Lewis, ££.§l¢ reported just the opposite and attributed the difference in the rate of conduction to the spiral or circular arrangement of the muscle fibers. They further concluded that the conduction rates of the musculature of the postcava are different from those in the precava, because of the longer "cuff" of fibers upon the inferior vena cava. Inferior Vena Cava Investigators who have continued to investigate the excitatory processes of the heart have reported cardiac muscle in the inferior vena cava. Keith (1903), in a comparison of the mammalian and reptilian embryos related that the right sinus venosus receives both the superior and inferior venae cavae. They are both surrounded by "loop-shaped" cardiac muscular fibers which stem from the heart. The extent of these cardiac fibers on the vessels was not determined. Robb (1934), and Papas (1920), reported that the distance to which cardiac musclesbundles of the atria continue onto the inferibr-vena cava varies.in hearts from different species. These fascicles of heart muscle usually end in fibrous bundles. It was also shown that the cardiac muscle bundles continuing downward over the inferior vena cava are not arranged in a circular pattern, as observed by most investigators in the precava. Thomas (1959), noted that cardiac muscle fibers continue onto the inferior vena cava of the hog and dog for approximately one centimeter and in no case beyond two centimeters. These cardiac fibers constitute the entire thickness of the caval wall. An investigation by Franklin (1932), on the thoracic inferior vena cava in rabbits and cats revealed that only connective tissue is present. There was no mention of the level at which the sections were taken but it is reasonable to assume that they were not close to the heart since other investigators, Keith (1903), Lewis gt 3;. (1914), Papez (1920), Robb (1934), and Thomas (1959), reported cardiac muscle continuing for some distance down the postcava in animals of different species. Trautmann and Fiebiger (1957), Krolling and Grau (1960), Copenhaver and Johnson (1958), and Maximow and Bloom (1957), stated that near the heart, the walls of large veins contain varying amounts of cardiac muscle fibers. Pulmonary Veins Flack (1910), completed a study on the S-A node. He found remnants of heart muscle extending from the sinus and continuing around the orifices of the pulmonary vein of the left auricle. In a report by Keith.and Flack (1907), it was related that in the heart of the frog embryo the cardiac musculature of the sinus at the S-A junction, includes the orifices of the pulmonary veins. It is possible, therefore, that the cardiac muscle of the sinus remains around the opening of the pulmonary veins in the adult stage. Keith (1903), working with the human species, had already established that contractions of the auricles cannot spread backward into the pulmonary veins because of the presence of "loop-shaped" cardiac muscle fibers at the openings of the pulmonary vessels. In addition, Keith found that the pulmonary veins lacked striated muscle fibers until they perforated the pericardium. Glomset and Glomset (1940), in a gross study noticed that the cardiac muscle fascicles of the pulmonary vessels have about the same arrangement as those of the superior vena cava. Papez (1920), was in complete agreement with this. He stated that some of the cardiac muscle bundles that extend onto the left pulmonary vein encircle the vessel in a radiate and somewhat circular manner. In addition, it was noted that all veins are covered by fascicles of heart muscle originating in the atria. Robb (1934), and Thomas (1959), agreed with their colleagues and reported that in the dog there are three pulmonary vessels and all contain cardiac muscle. Smith and Calhoun (1960), found cardiac muscle in the wall of the pulmonary veins extending into the lung of the albino rat. Arey (1954), Copenhaver and Johnson (1958), and Maximow and Bloom (1957), reported cardiac muscle extending for a distance into the pulmonary veins in man. Pulmonary Artery and Aorta Bremer and Weatherford (1946), described short, broad, flat muscle cells "somewhat resembling cardiac muscle" in the aorta. Arey (1957), and many other investigators have noted heart muscle in the roots of the aorta and pulmonary artery. This is to be expected since the roots of these vessels have been incorporated in the heart during the developmental period. No other reference to cardiac muscle in either the pulmonary artery or aorta has been found. 8 Although this study has not taken into consideration the coronary arteries it has recently been shown by Polacek (1959), that the coronary arteries are "over-bridged" by muscle bundles of ventricular or atrial myocardium. MATERIALS AND METHODS For this study the heart and surrounding blood vessels of twelve dogs were used. Included in this group were six female and four male mongrel type dogs and one male purebred poodle. These animals were obtained from the departments of Anatomy,and Surgery and Medicine at Michigan State University. The hearts from five freshly killed animals were fixed in mercury- formol-saline solution (Dawson and Friedgood, 1938), or formalin-alcohol- acetic acid (Lavdowsky's) mixture (Guyer 1949). The other seven were embalmed specimens injected with latex. Longitudinal sections were taken from the superior and inferior vena cava, pulmonary vein, azygos vein, pulmonary artery and aorta. The sections were dehydrated in dioxane, embedded in paraffin and sectioned at 8 microns. The extension of cardiac muscle into the veins and arteries was measured with a calibrated ocular micrometer. Statistical analysis of the measurements in Table I were outlined by using the "t" test. , Three different staining techniques were used. Hematoxylin and eosin were used to facilitate the study of muscle, Weigert's and VanGiesen's and Crossman's modification of Mallory's connective tissue stain aided the study of the connective tissues. 10 RESULTS AND DISCUSSION Superior Vena Cava Extent. In medium sized mongrel-type dogs cardiac muscle extended for distances ranging from 1.58 to 2.38 centimeters in both sexes. The average distances were 1.85 and 1.90 centimeters for males and females respectively. In a small dog (poodle), cardiac muscle extended for only 1.35 centimeters while in a larger animal (shepherd-type) cardiac muscle fibers extended for 3.05 centimeters. The average extension of cardiac muscle in all dogs, regardless of type or sex was 2.04 centimeters. Papez (1920), and Keith (1903), reported similar findings on dog and man. A The widths of cardiac muscle was measured as close to the heart as possible and at intervals of 4.2 mm thereafter to its terminal point. As can be seen in Table I, the cardiac muscle band tapered to an average width of .14 mm at its termination. The widths at corresponding points were somewhat greater in the females than in the males. The average width at the point nearest the heart being .09 mm in the females compared to .71 mm in the males. In the poodle the width nearest the heart was .49 mm while in the large shepherd type it was 1.27 mm. Arrangement. In the dog cardiac muscle was continuous from the wall of the atrium into the wall of the superior vena cava. Near the heart cardiac muscle is arranged in an inner and outer circular manner with a layer of longitudinal fibers between (PLATE I). A few muscle bundles were spiral and therefore appeared oblique in sections. The longi- tudinal bundles dwindlediout in the first'centimeter or so from the 11 heart, while the mixed circular and spiral bundles remained to the termination (PLATE III, IV). Termination. The cardiac muscle fibers in the superior vena cava ended in fibrous tissue. Elastic and white fibrous connective tissue extended between the muscle bundles and appeared to invest the tapered muscle fiber in some places (PLATE III). Azygos Vein Extent. Measurements of the extension of cardiac muscle along the wall of the azygos vein were taken from a point as near as possible to ,its junction with the superior vena cava. Cardiac muscle extended for distances ranging from 4.07 mm to 7.64 mm in medium sized mongrel-type dogs. The average measurement for the males was 6.65 mm while the females averaged 6.12 mm. In the poodle cardiac fibers extended 6.90 mm and in the shepherd type 9.26 mm. The average extent for all dogs was 7.23 mm. The width of the cardiac muscle at the junction of the azygos vein and the superior vena cava averaged .19 mm in males and .16 mm in the females of mongrel type. In the poodle the range was from .13 mm to .32 mm in the shepherd type. 'The average distance that cardiac muscle extended along the azygos vein in all the dogs in thus study was .19 mm. Arrangement. Cardiac muscle continued.from the superior vena cava onto the wall of the azygos vein (PLATE V). In some places the muscle appeared to extend only in a circular direction (PLATE VI).. The cardiac muscle in the vena azygos terminated by dwindling out (PLATE VII). 12 Termination. While many elastic fibers were present and extended along the cardiac muscle fibers, the fibrillae themselves seemed to attach to prominent collagenous bundles (PLATE VII). Inferior Vena Cava Extent. Cardiac muscle extended for distances ranging from 7.35 mm to 9.71 mm in dogs of the same type with the average distance for both sexes being 8.59 mm. In a poodle the extent was 7.05 mm and in the shepherd type it was 13.67 mm. The average extent for all dogs used was 9.48 mm. The width of the cardiac muscle mass in the mongrel-type dog at the point nearest the heart averaged .67 mm in the males and .65 mm in the females. The same point measured .61 mm in the poodle and .98 in the larger type dog. The average width of cardiac muscle in the inferior vena cava was .72 mm. Arraggement. The inferior vena cava was characterized by a cardiac muscle sheath (PLATE VIII). Near the heart the bundles were arranged both circularly and spirally (PLATE IX).. PLATE X shows the? junction of the inferior vena cava with a vasa vasorum. Termination. Elastic and white fibrous connective tissue fibers were present at the termination of cardiac muscle in the inferior vena cava. Elastic fibers were more concentrated around the ends of the cardiac muscle than at other places in the wall of the cava. In.many places there was a connection between the elastic fibers and the investing coat of the cardiac muscle. At several places elastic fibers coursed between the bundles of muscle (PLATE XI). 13 Pulmonary Veins Extent. Fascicles of cardiac muscle were present in the pulmonary veins but did not extend as far as the lung in any of the dogs observed in this study (PLATE XII). Cardiac muscle was present for distances ranging from 1.10 mm to 8.08 mm in mongrel-type dogs. The extent in the poodle was 7.64 mm and in the shepherd type 12.20 mm. The average distance which cardiac muscle extended in all animals used regardless of type or sex was 7.58 mm. The widths of the cardiac muscle nearest the heart were .57 mm and .44 mm in the male and female mongrels respectively. The widths in the poodle and larger shepherd type were .47 mm and 1.49 mm with an over-all average of .74 mm for all animals. Arrangement. Cardiac muscle did not end abruptly at the openings of the pulmonary veins into the heart. Atrial heart muscle was continuous onto the walls of the pulmonary veins. Near the entrance to the heart the cardiac muscle was arranged in an outer and inner circular pattern with a few middle longitudinal bundles ( PLATE XIII). The muscle arrangement here is similar to that of the superior vena cava. This agrees with the work of Glomset and Glomset (1940). Distal to this point and extending to its termination the outer circular muscle was absent, leaving outer longitudinal and inner circular layers (PLATE XIV). Termination. Elastic and collagenous fibers were present at the terminal point of the cardiac muscle in the pulmonary vein. (PLATE XV). The elastic fibers closely invested the tips of the muscle fascicles but did not penetrate the muscle mass as it did in the venae cavae. White fibrous 14 tissue was in greater proportion to elastic fibers than in the other vessels. Pulmonary Artery and Aorta Cardiac muscle did not extend onto the pulmonary artery or aorta (PLATES XVI, XVII). A fibrous connective tissue band was present in the wall of the pulmonary artery at its exit from the heart (PLATE XVI). Malewitz and Calhoun (1958), investigated this region in the turkey and reported white fibrous cartilage at the junctions of the pulmonary artery and aorta with the heart. The elastic and smooth muscle fibers in the wall of the aorta end in white fibrous tissue. There is no apparent continuity of these fibers with the cardiac muscle of the heart (PLATE XVII). 15 SUMMARY AND CONCLUSIONS A histological study was undertaken to determine the presence, extent and arrangement of cardiac muscle in the venae cavae, azygos vein, pulmonary veins, pulmonary artery and aorta in the dog. Cardiac muscle was found in the venae cavae, pulmonary veins and azygos vein, but was absent from the pulmonary artery and aorta. Statistically there were no significant sex or breed differences in the extent of cardiac muscle in any of these vessels. The average distances to which cardiac muscle coursed in the superior vena cava, inferior vena cava,pulmonary vein and azygos vein of‘all the animals used were 2.04 cm, .948 cm, .758 cm, and .723 cm respectively.{ Measurements indicated.that the cardiac muscle mass gradually narrowed between the heart and the terminal point. The cardiac muscle pattern in the superior vena cava and pulmonary veins was very similar. 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