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Distribution and Structure of Purkinje Fibers in the Heart of Ostrich (Struthio camelus) with the Special References on the Ultrastructure

Distribution and Structure of Purkinje Fibers in the Heart of Ostrich (Struthio camelus) with the... Hindawi Publishing Corporation International Journal of Zoology Volume 2013, Article ID 293643, 6 pages http://dx.doi.org/10.1155/2013/293643 Research Article Distribution and Structure of Purkinje Fibers in the Heart of Ostrich (Struthio camelus) with the Special References on the Ultrastructure 1 2 2 3 Paria Parto, Mina Tadjalli, S. Reza Ghazi, and Mohammad Ali Salamat Biological Department, Faculty of Science, Razi University, Kermansha 6714967346, Iran School of Veterinary Medicine, Shiraz University, Shiraz 1731-71345, Iran Biological Department, Faculty of Science, Razi University, Kermansha 6714967346, Iran Correspondence should be addressed to Paria Parto; pariaparto@gmail.com Received 20 May 2013; Revised 29 July 2013; Accepted 29 July 2013 Academic Editor: Greg Demas Copyright © 2013 Paria Parto et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Purkinje fibers or Purkinje cardiomyocytes are part of the whole complex of the cardiac conduction system, which is today classified as specific heart muscle tissue responsible for the generation of the heart impulses. From the point of view of their distribution, structure and ultrastructural composition of the cardiac conduction system in the ostrich heart were studied by light and electron microscopy. These cells were distributed in cardiac conducting system including SA node, AV node, His bundle and branches as well as endocardium, pericardium, myocardium around the coronary arteries, moderator bands, white fibrous sheet in right atrium, and leftseptalattachmentofAVvalve.ThegreatpartofthePurkinjefiberiscomposedofclear,structurelesssarcoplasm,andthemyobfi - rils tend to be confined to athin ring around theperiphery of thecells.They have oneormorelarge nuclei centrally locatedwithin the be fi r. Ultrastructurally, they are easily distinguished. eTh main distinction feature is the lack of electron density and having a light appearance, due to the absence of organized myob fi rils. P-cells usu ally have two nuclei with a mass of short, delicate microfilaments scattered randomly in the cytoplasm; they contain short sarcomeres and myofibrillar insertion plaque. eTh y do not have T-tubules. 1. Introduction This is the arterioventricular node. In addition, he was able to display interdigitating connections between the Purkinje Jan Evangelista Purkinje was born on 18 December, 1787, fibers and ventricular muscles, as well as between the node in Libochovice (Bohemia). Between the ages of 35 and 63, and arterial muscles [2]. Electrical activity of the specialized he made his most significant discoveries. This very age conducting system of canine hearts has been recorded in situ generally displays the physiological measure of the biggest through electrodes attached to the endocardium during total creative waves of the human being. From 1850 until his cardiopulmonary bypass [3]. Armiger et al. [4]statedthat death in 1869, Purkinje worked in the Institute of Physiology the connective tissue of the trabeculae got from the puppies in Prague,which he hadbased.Theacquisition of thebig and the young dogs had little elastic b fi ers, but this element Plo¨sl microscope in 1835 represented an important turning was well extended in the connective tissue of the adult dogs. point for Purkinje’s histological and embryological research. The trabeculae of older dogs also showed distributed foci of Purkinje published his discovery of a part of the heart con- extracellular fat droplets, and their junctional areas nearest duction system, nowadays called Purkinje fibers or Purkinje to the ventricular wall were oen ft heavily full with fat. eTh cardiomyocytes [1]. Purkinje cells were uniform in each group but differed from Tawara (1906) was able to follow proximally from the one group to another [4]. Purkinje fibers (P-fiber) to the besides bundles, which, he organize, were connected to his bundle. Aeft rwards, he Forsgren et al. [5] identified that in the bovine fetal heart found that his bundle was connected proximally to a well- subendocardial bundles of cells could be prominent from the set plexus of b fi ers (which he called a node, in his book). main myocardial mass. eir Th morphological characteristics 2 International Journal of Zoology Figure 1: Photomicrograph from the microscopic location of the Figure 3: Photomicrograph from the microscopic location of the Purkinje cell in the endocardial layer of the sinus venosus of left Purkinje fibers (P) around coronary artery (A), between the heart sinus—arterial valve in the male ostrich heart. Arrow—myob fi ril muscle bundles, (M) Green Masson’s Trichrome. cells. the right ventricle and gives attachment to its rough parietal wall by a thick muscular stalk. The left and right pulmonary SE veins enter the left atrium independently, and their openings SA were completely separated from each other by a septum. In the heart of the ostrich, the moderator bands were found in both the right and left ventricles in different locations. The L → right ventricle presents one tendinous moderator band near thebaseofthe ventriclethatextends from septum to themus- cular valve. Also the moderator bands as tendinous thread like or flat sheet are usually present at about apex of the right ventricle that extends from septum to the parietal wall. In the left ventricle, there were some tendinous moderator bands close to the apex that extends from septum to the parietal wall Figure 2: Photomicrograph from the microscopic location of the and between trabeculae carneae of the parietal wall [7]. Purkinje fibers in endocardium, that showing the layers, Green Mas- Cardiovascular diseases in human and animals are one of son’s Trichrome. Arrow—endothelium cells, SE—subendothelium the main causes of death. u Th s, correct interpretation of heart layer, SA—subendocardial, P—Purkinje cell, —connective tissue sheath,M—myocardialcells,L—lipofuscinpigment. function or physiology needs full understanding of anatomy, histology, and cardiac conduction system. Macroscopic and microscopic anatomy of heart and its conduction system has been studied in several animal species, but there is no express that they represent bundles of Purkinje fibers. A comprehensive research on the ostrich (Struthio camelus) severe u fl orescence after incubation in antisera up to the heart. The results of this survey in future will be used as basic intermediate filament protein skeleton is also backing this knowledge. suggestion [5]. A comparative ultrastructural study of bovine Purkinje fibers and common myocytes during fetal development has 2. Materials and Methods been undertaken by Forsgren and Thornell [ 6]. Differences between the two cell types with respectability 2.1. Light Microscopy. Five hearts from healthy male ostriches to the accommodated disc, amount of myobfi rils, sequence were used. eTh hearts were collected at the slaughter house of mitochondria, amount of glycogen, and formation of T- immediately aeft r slaughter. eTh average weight of the hearts tubules became apparent gradually. In all stages studied, a was 1054.33± 172.34 g; the length of the long axis was 19.33 redundancy of intermediate filaments was typical for the ± 1.05 cm; and the circumferential length at the coronary Purkinje fibers. Myob fi rillar M-bands developed an ear- groove was 35.66± 1.04 cm. Aeft r removal of pericardium, lier stage in Purkinje b fi res than in ordinary myocytes. the hearts were ushe fl d with normal saline and subse- Myofilament-polyribosome complexes typical of adult cow quently immersed in 10% bueff r neutral formalin for 72 hrs Purkinje fibers were not seen in the fetal hearts [ 6]. (ventricular apex was cut off to permit the penetration of The ostrich heart has some different features from the formalin into the lumen). eTh right and left atrium, right other birds. In the ostrich, fibrous pericardium as sternoperi- muscular valve, and interarterial septum were separated and cardial ligament attaches along the thoracic surface of the divided into several segments. Each segment was dehydrated, sternum. eTh central edge of muscular valve hangs down into cleared, and embedded in paraffin. Serial sections of 6–8 Lm International Journal of Zoology 3 (a) (b) Figure 4: (a) Photomicrograph from the microscopic location of the b fi rous white sheet in between the pectinate muscles (PE), in the right atrium (RA) in the male ostrich heart. Green Masson’s Trichrome: CT—connective tissue mass, CO—columns of Purkinje cells. (b) Photomicrograph from the microscopic location of the b fi rous white sheet (WP) and related clauses (arrow) in right atrium the male ostrich heart: RA—right atrium bottom, PE—shoulder muscles. than normal muscle fiber, about 5.5–16 𝜇 m. The arrangement of the component in P-b fi er is different from cardiac muscle fibers. The great part of the fiber is composed of clear, struc- ture less sarcoplasm, and the myofibrils tend to be confined to a thin ring around the periphery of the cells. They have one or more large nuclei centrally located within the b fi er (Figure 1). P-bfi er in the heart of the ostrich was distributed widely. Throughout the endocardial layers, particularly the subendocardial layer, numerous P-fibers, arranged in one or more rows, are seen (Figure 2). In the myocardium, between muscles bundles, the P-fibers are seen. Passing outwards from the network of P-bfi ers lying in the endothelial layer, there are large numbers of conduction b fi er tracts. These tracts Figure 5: Photomicrograph from the microscopic location of the divide up, passing between the muscle fiber bundles, and sinoatrial node (SAN), showing P cells (P), transitional cells (T), and eventually the nes fi t divisions of the tracts, single Purkinje intermediate (I). Arrow—endothelial cells in surface sinuatrial valve bfi ers, are found within the bundles in close association of the sinus venosus, Green Masson’s Trichome. with the muscle be fi rs. eTh se be fi r tracts are usually found in association with the branches of the coronary arteries (Figure 3). The P-fibers are occasionally seen in epicardial layer but occurs lie in protrusion of epicardium below of the thickness were cut, mounted, and stained with H&E and surface of myocardium around coronary arteries. In the right Green Masson’s Trichrome [8]. auricleofthe ostrichheart,P-bfi ers arefound mostextenely beneath the endocardium as a single fibre or well-developed 2.2. Electron Microscopy. Three other hearts were removed tracts.Theselatterare foundmostfrequentlyinthe junction just aer ft slaughter and quickly immersed in Karnovsky’s of auricle with right atrium, and macroscopically they are solution for xfi ation. Cubes of tissue (about 1 mm) were with fibers sheet in this junction ( Figure 4). post-fixed in 1% osmium tetroxide with 0.1 m phosphate eTh conducting system of the heart (sinoatrial node, bueff r. Specimens were dehydrated in ethanol and embedded arterioventricular node his bundle and its branches) consists in epoxy resin. Thin sections (0.5–1 Lm) were stained with of these b fi ers. eTh structure of P-fiber varies according to the toluidine blue to identify the location of AV node. Ultra- part of conducting system in which they occur. eTh sinoatrial thin sections (600A ) were mounted on the copper grids node is composed of P-fibers and intermediate fibers (the and stained with uranyl acetate and lead citrate and were fibers which, in appearance, are intermediate between P- examined with a Philips CM-10 electron microscope, and bfi ersand cardiacmusclefibers). P-bfi ersare locatedinthe electromicrographs were prepared. peripheral region of this node and passing away from it. In the initial stages of their passage away from the node, they have a thick connection tissue sheet (Figure 5). 3. Results The atrioventricular node is composed of fibers which Purkinje fibers in the ostrich heart are large specialized resemble P-b fi er more closely than the myocardial muscle cardiac muscle b fi ers. eTh y have a much greater diameter fibers. Posteriorly, the AV-node narrows down somewhat and 4 International Journal of Zoology CT AVB AVN Figure 8: Photomicrograph from the microscopic location connect- Figure 6: Indicative junction of the arterioventricular node (AVN) ing the left stalk in the connecting area to atrioventricular valve. and arterioventricular bundle (AVB) in the male ostrich heart. CT—connective tissue mass, P—Purkinje cells, E—elastic b fi ers, Green Masson’s Trichrome. F—fibroblast cell, C—collagen fibers, P—parietal wall of the right ventricle; H&E. RA FR AM ∗ MS IV P Figure 7: Photomicrograph from the microscopic location of the Figure 9: The heart of male ostrich, showing the anatomical Purkinje cells( ) in arterioventricular of bundle (AVB) in the male location of the atrioventricular valve. FR—bfi rous ring, RA—right atrium, IV—interventricular septum, M—right muscular valve, ostrich heart. C—collagen b fi ers, arrow—fibroblast; Green Masson’s Trichrome. MS—muscular stalk, AM—connect the left stalk. 4. Discussion continues as the arterioventricular (His) bundle (Figure 6). This bundle itself is composed of a large number of P- The distribution of Purkinje fibers has been studied in various fibers. Three bundle branches (right/left and recurrent) are mammals. In mammals, the Purkinje network is distributed consisting of P-fibers which are arranged as a cord ( Figure 7). in the subendocardial connective tissue in ventricle. es Th e The moderator bands, which are found in the right and networks conduct the cardiac excitation from right and left left ventricle of the ostrich’s heart, consist of only dense his bundle to the myocardium. In human and dogs, the irregular connective tissue, and the Purkinje cells fill the core Purkinje cell in the network is cylindrical or fusiform in shape of moderator bands. There was cell-to-cell communication and arranged in a parallel pattern [9]. In ungulates (sheep and between Purkinje be fi rs within the bundle. eTh Purkinje cells goat), the chain of Purkinje cells was larger than myocytes, were surrounded by connective tissue sheath (Figure 8). and 2–8 oval cells formed these network. The cells connect eTh thick muscular stalk attached the peripheral edge of to each other by desmosomes and gap junction. These cells themuscularrightAVvaluetothearterio-ventricularseptum are covered by a thick sheath of reticular b fi ers [ 10]. In rat and rough parietal wall of the ventricle. Histologically it is and mice, Purkinje cells were very similar to ventricular composed of Purkinje fibers ( Figure 9). myocytes even a little smaller. eTh y are cylindrical in shape With the electron microscopy, the P-cell is easily distin- and organized in parallel pattern, continuing with ventricular guished. The main distinction feature is the lack of electron myocytes in the endocardium [11]. density and having a light appearance, due to the absence of Various aspects of the histochemistry of Purkinje b fi ers organized myofibrils. P-cells usually have two nuclei with a have been studied by Getty [12]and Gossrau[13]. The obser- mass of short, delicate microfilaments scattered randomly in vations of DiDio [14], Hirako [15], and Sommer and Johnson the cytoplasm; they contain short sarcomeres and myofibril- [16] on the general morphology of the ordinary and Purkinje lar insertion plaque. eTh y do not have T-tubules ( Figure 10). cells of the fowl heart have been confirmed. The Purkinje cells International Journal of Zoology 5 (a) (b) Figure 10: (a) Electromicrograph of two P cells (P) represents the folded membrane (arrow), nucleus (N), myofibrils (M), and mitochondrial (Mt). (b) Electromicrograph part of the P cell, showing leptomer (L), along myob fi ril (M). of the fowl are similar in almost all aspects to those of mam- deep into the interventricular septum and then bifurcate mals.They do nothavestep-like intercalated discsbut have into right and left limb. The later branch divides up from irregularly arranged areas of membrane apposition, which the network of P-fibers. Prakash’s [ 19] description does not possess desmosomes, myob fi rillar insertion plaques, and exactly coincide with that of DiDio [14]for thepigeonand large pentalaminar nexuses. No transverse tubular system is swan but resemble more closely to that of Drennan [21]for present, and the sarcoplasmic reticulum is poorly developed. the Ostrich. Similarly, the description of Yousuf [22]for the eTh few myofibrils are irregularly arranged. eTh Purkinje heartofpasserdieff rsinthe basicstructure of this part of the cellshavebeenobservedinthisstudy to containrounded conducting system. aggregations of leptomeres. Leptomeres have previously been One of the features of specific interest in the ostrich heart described by Hirako [15] who suggested that they represented is the presence of moderator bands in both the right and left an aberrant form of muscle bfi ril arising during development. ventricles and in different locations. eTh right ventricle has Thisisunlikelysince they arepresent in almost allPurkinje one tendinous moderator band about the base of the ventricle cells. that extends from the septum to the muscular valve. Also the It seems reasonable to assume that they are associated moderator bands are usually about apex of the right ventricle with myofibrillar formation or destruction since they are seen that extend from septum to parietal wall. In the left ventricle, in association with large masses of disorganized filaments there were some tendinous moderator bands close to the andalsoincontinuitywithapparentlynormalmyobfi rils. apex that extend from septum to parietal wall and between The conducting system consists of the sinoatrial node, the trabeculae carneae of parietal wall. The moderator bands atrioventricular node and bundles, and highly complex net- tend to prevent over distension and serve as the pathway for work of n fi e bundles and tracts [ 16]. Although SA node has the passing of Purkinje fibers across the lumen of the cavity been demonstrated in other birds, there is still some doubt forming a part of the conducting system. Anatomically, the as to its position and even its presence as a discrete node in location of the moderator band in the right and left ventricle birds [17]. Concluded from physiological evidence that an SA of the ostrich heart is different from the other animals. er Th e node was present near the termination of the right precaval were no papillary muscle in the right ventricle of the ostrich vein.Thenodeinanostrich heartiscomposedoffibers, and the moderator band attaches directly to the ventral which in appearance are intermediate between muscle b fi ers surface of muscular valve from interventricular septum. andtruePurkinjefibers.Peripherallywithinthe node and Since in human [23, 24] the moderator band extends passing away from it are several true P-fibers. eTh distribution between interventricular septum and ventricular free wall of P-fibers within the auricles in ostrich heart is similar to and in domestic animals [25]and ungulates[26]these bands that described by Davis [18]for thepigeon. Prakash[19]has extend from interventricular septum to the papillary muscle stated that the atria are devoid of P-be fi rs. In our study, they andthere is no connection to thevulvarcusps.Inthe Ostrich arefound within themyocardiuminassociation with blood left ventricle, despite the presence of papillary muscle, these vessels, and occasionally in the epicardium [20]. Davis [18] bands have no connection to them. Histologic structure of stated that the auricular P-b fi ers stop short at the base of the moderator band showed that they have muscular tissue in auricles and that there are no interconnections between them various proportions with connective and conductive tissue and the reminder of the cardiac conducting system. [27]. It is similartothatofthe human[28], ungulate [26], Intheostrich,theAV-nodeliesinthebaseoftheauricular sheep [24, 29]and goat [24]heartsbut in thecarnivores, septum. It is very close to the junction of the auricular and a real moderator band was never found [26]. Whatever is ventricular septa. It is composed of b fi ers which resemble P- the size and shape, the moderator band must be regarded bfi ersmoreclosely than themyocardialmusclefibres andthat as the shortest pathway from interventricular septum to the they are not identical to those of the SA-node. As Prakash free wall of left and right ventricle in the ostrich and other [19] reported, the atrioventricular bundle in our study extend animals. The Purkinje fibers are large in size and similar in 6 International Journal of Zoology most cellular characteristics in ostrich and dog [30], but in [14] L. J. DiDio, “Myocardial ultrastructure and electrocardiograms of the hummingbird under normal and experimental condi- the ostrich, there is no perinuclear clear area. eTh re is a little tions,” Anatomical Record,vol.159,no. 4, pp.335–352,1967. glycogen in these cells, but in human and mammals these cells [15] R. Hirako, “Fine structure of Purkinje fibers in the chick heart,” arerichinglycogen[4]. The Purkinje fibers are organized Archivum Histologicum Japonicum,vol.27, no.1,pp. 485–499, into the bundle with cell-to-cell communication and little lateral communication. In the ostrich, there is a sheath of [16] J. R. Sommer andE.A.Johnson,“Cardiacmuscle—acompar- connective tissue around the Purkinje cells, but in human and ative ultrastructural study with special reference to frog and mammals there is no b fi rous sheath around these cells [ 25]. chicken hearts,” Zeitschrift f u¨r Zellforschung und Mikroskopische This organization of the bundle fibers increases the spread Anatomie, vol. 98, no. 3, pp. 437–468, 1969. of propagated impulses and inhibits the transverse spread. In [17] E. Mangold and T. Kato, “Zur vergleichenden Physiologie des the right ventricle, there is one musculotendinous moderator ¨ ¨ His’schen Bundels,” Pfl ugers Archiv,vol.160,pp. 91–131,1914. band about the base of the ventricle, which extends from the [18] F. Davis, “eTh conducting system of the bird’s heart,” Journal of interventricular septum to the muscular stalk of the muscular Anatomy,vol.64, pp.129–146,1930. valve. It was single and sometimes branched [4]. [19] R. Prakash, “eTh heart and its conducting system in the common Indian fowl,” Proceedings of the National Institute of Acknowledgment Sciences of India,vol.22, pp.22–27,1956. [20] R. C. Truex, Comparative Anatomy and Functional Consider- eTh authors are grateful to the research council of the Shiraz ation of the Cardiac Conducting System, Elsevier, Amsterdam, University for providing financial assistance. The Netherlands, 1961. [21] M. R. Drennan, “eTh auriculo-ventricular bundle in the bird’s heart,” British Medical Journal,vol.1,pp. 321–322, 1927. References [22] N. Yousuf, “The conducting system of the heart of the house [1] O. Eliˇska, “Purkynje b fi ers of the heart conduction system— sparrow, Passer domesticus indicus,” Anatomical Record,vol. history and the present time,” Casopis Lekaru Ceskych,vol.145, 152, no. 3, pp. 235–249, 1965. no. 4, pp. 329–335, 2006. [23] A. K. Abdulla, A. Frustaci, J. E. Martinez, R. A. Florio, J. [2] S. Tawara, Das Reizleitungssystem des Saugetierhezens,Verlag Somerville, and E. G. J. Olsen, “Echocardiography and pathol- von Gustav Fischer, Jena, Germany, 1906. ogy of left ventricular “false tendons”,” Chest, vol. 98, no. 1, pp. 129–132, 1990. [3] B.F.Hoffman, P. F. Cranefield, J. H. Stuckey, andA.A.Bag- danas, “Electrical activity during the P-R interval,” Circulation [24] M. Deniz, M. Kilinc¸, and E. S. Hatipoglu, “Morphologic study Research, vol. 8, pp. 1200–1211, 1960. of left ventricular bands,” Surgical and Radiologic Anatomy,vol. 26,no. 3, pp.230–234,2004. [4] L.C.Armiger,F.Urthaler, andT.N.James,“Morphological changes in the right ventricular septomarginal trabecula (false [25] R. Depreux, H. Mestdagh, and M. Houcke, “Comparative tendon) during maturation and ageing in the dog heart,” Journal morphology of the trabecula septomarginalis in terrestrial of Anatomy, vol. 129, no. 4, pp. 805–817, 1979. mammals,” Anatomischer Anzeiger,vol.139,no. 1-2, pp.24–35, [5] S. Forsgren, L. E. Thornell, and A. Eriksson, “eTh development of thePurkinjefibresysteminthe bovine fetalheart,” Anatomy [26] D. Lotkowski, M. Grzybiak,D.Kozłowski,K.Budzyn,and W. and Embryology,vol.159,no. 2, pp.125–135,1980. Kuta, “A microscopic view of false tendons in the left ventricle of the human heart,” Folia morphologica,vol.56, no.1,pp. 31–39, [6] S. Forsgren and L. E. Thornell, “eTh development of Purkinje fibres and ordinary myocytes in the bovine fetal heart. An ultrastructural study,” Anatomy and Embryology,vol.162,no. 2, [27] P. Parto, M. Tadjalli, and S. R. Ghazi, “Macroscopic and pp.127–136,1981. microscopic studies on maderator bands in the heart of ostrich (struthio camelus),” Global Veterinaria,vol.4,no. 4, pp.374–379, [7] M. Tadjalli, S. R. Ghazi, and P. Parto, “Gross anatomy of the heart in Ostrich (Struthio camelus),” Iranian Journal of Veterinary Research,vol.10, no.1,pp. 21–27, 2009. [28] R. I. Clelland, “Note on a moderator band in the left ventricle and perforate septum ovale in the heart of a sheep,” Journal of [8] L. G. Luna, Manual of Histologic Staining Methods of the Armed Anatomy and Physiology,vol.32, no.4,p.779,1898. Forces Institute of Pathology, American Registry of Pathology, New York, NY, USA, 3rd edition, 1968. [29] G. E. Sandusky Jr. and S. L. White, “Scanning electron microscopy of the canine atrioventricular bundle and moder- [9] P.F.Cranefield,A.L.Wit,and B. F. Hoffman,“Conduction of ator band,” American JournalofVeterinaryResearch,vol.46, no. the cardiac impulse. 3. Characteristics of very slow conduction,” 1, pp. 249–252, 1985. Journal of General Physiology,vol.59, no.2,pp. 227–246, 1972. [30] R. C. Truex and W. M. Copenhover, “Histology of the moderator [10] T. Shimada, T. Ushiki, and T. Fujita, “Purkinje fibers of the band in man and other mammals with special reference to the heart,” Shinyaku to Chiryou,vol.42, pp.11–13,1992. conduction system,” American Journal of Anatomy,vol.80, no. [11] Sawazaki, Hikaku Sinzougaku,Asakura Shoten,1985, 2, pp. 173–201, 1947. (Japanese). [12] R. Getty, Sisson and Grossman’s, the Anatomy of the Domestic Animals,WBSaunders, 5thedition,1975. [13] R. Gossrau, “eTh impulse conducting system of the birds— histochemical and electron microscopical investigations,” His- tochemie,vol.13, no.2,pp. 111–159,1968. 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Distribution and Structure of Purkinje Fibers in the Heart of Ostrich (Struthio camelus) with the Special References on the Ultrastructure

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Copyright © 2013 Paria Parto et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Hindawi Publishing Corporation International Journal of Zoology Volume 2013, Article ID 293643, 6 pages http://dx.doi.org/10.1155/2013/293643 Research Article Distribution and Structure of Purkinje Fibers in the Heart of Ostrich (Struthio camelus) with the Special References on the Ultrastructure 1 2 2 3 Paria Parto, Mina Tadjalli, S. Reza Ghazi, and Mohammad Ali Salamat Biological Department, Faculty of Science, Razi University, Kermansha 6714967346, Iran School of Veterinary Medicine, Shiraz University, Shiraz 1731-71345, Iran Biological Department, Faculty of Science, Razi University, Kermansha 6714967346, Iran Correspondence should be addressed to Paria Parto; pariaparto@gmail.com Received 20 May 2013; Revised 29 July 2013; Accepted 29 July 2013 Academic Editor: Greg Demas Copyright © 2013 Paria Parto et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Purkinje fibers or Purkinje cardiomyocytes are part of the whole complex of the cardiac conduction system, which is today classified as specific heart muscle tissue responsible for the generation of the heart impulses. From the point of view of their distribution, structure and ultrastructural composition of the cardiac conduction system in the ostrich heart were studied by light and electron microscopy. These cells were distributed in cardiac conducting system including SA node, AV node, His bundle and branches as well as endocardium, pericardium, myocardium around the coronary arteries, moderator bands, white fibrous sheet in right atrium, and leftseptalattachmentofAVvalve.ThegreatpartofthePurkinjefiberiscomposedofclear,structurelesssarcoplasm,andthemyobfi - rils tend to be confined to athin ring around theperiphery of thecells.They have oneormorelarge nuclei centrally locatedwithin the be fi r. Ultrastructurally, they are easily distinguished. eTh main distinction feature is the lack of electron density and having a light appearance, due to the absence of organized myob fi rils. P-cells usu ally have two nuclei with a mass of short, delicate microfilaments scattered randomly in the cytoplasm; they contain short sarcomeres and myofibrillar insertion plaque. eTh y do not have T-tubules. 1. Introduction This is the arterioventricular node. In addition, he was able to display interdigitating connections between the Purkinje Jan Evangelista Purkinje was born on 18 December, 1787, fibers and ventricular muscles, as well as between the node in Libochovice (Bohemia). Between the ages of 35 and 63, and arterial muscles [2]. Electrical activity of the specialized he made his most significant discoveries. This very age conducting system of canine hearts has been recorded in situ generally displays the physiological measure of the biggest through electrodes attached to the endocardium during total creative waves of the human being. From 1850 until his cardiopulmonary bypass [3]. Armiger et al. [4]statedthat death in 1869, Purkinje worked in the Institute of Physiology the connective tissue of the trabeculae got from the puppies in Prague,which he hadbased.Theacquisition of thebig and the young dogs had little elastic b fi ers, but this element Plo¨sl microscope in 1835 represented an important turning was well extended in the connective tissue of the adult dogs. point for Purkinje’s histological and embryological research. The trabeculae of older dogs also showed distributed foci of Purkinje published his discovery of a part of the heart con- extracellular fat droplets, and their junctional areas nearest duction system, nowadays called Purkinje fibers or Purkinje to the ventricular wall were oen ft heavily full with fat. eTh cardiomyocytes [1]. Purkinje cells were uniform in each group but differed from Tawara (1906) was able to follow proximally from the one group to another [4]. Purkinje fibers (P-fiber) to the besides bundles, which, he organize, were connected to his bundle. Aeft rwards, he Forsgren et al. [5] identified that in the bovine fetal heart found that his bundle was connected proximally to a well- subendocardial bundles of cells could be prominent from the set plexus of b fi ers (which he called a node, in his book). main myocardial mass. eir Th morphological characteristics 2 International Journal of Zoology Figure 1: Photomicrograph from the microscopic location of the Figure 3: Photomicrograph from the microscopic location of the Purkinje cell in the endocardial layer of the sinus venosus of left Purkinje fibers (P) around coronary artery (A), between the heart sinus—arterial valve in the male ostrich heart. Arrow—myob fi ril muscle bundles, (M) Green Masson’s Trichrome. cells. the right ventricle and gives attachment to its rough parietal wall by a thick muscular stalk. The left and right pulmonary SE veins enter the left atrium independently, and their openings SA were completely separated from each other by a septum. In the heart of the ostrich, the moderator bands were found in both the right and left ventricles in different locations. The L → right ventricle presents one tendinous moderator band near thebaseofthe ventriclethatextends from septum to themus- cular valve. Also the moderator bands as tendinous thread like or flat sheet are usually present at about apex of the right ventricle that extends from septum to the parietal wall. In the left ventricle, there were some tendinous moderator bands close to the apex that extends from septum to the parietal wall Figure 2: Photomicrograph from the microscopic location of the and between trabeculae carneae of the parietal wall [7]. Purkinje fibers in endocardium, that showing the layers, Green Mas- Cardiovascular diseases in human and animals are one of son’s Trichrome. Arrow—endothelium cells, SE—subendothelium the main causes of death. u Th s, correct interpretation of heart layer, SA—subendocardial, P—Purkinje cell, —connective tissue sheath,M—myocardialcells,L—lipofuscinpigment. function or physiology needs full understanding of anatomy, histology, and cardiac conduction system. Macroscopic and microscopic anatomy of heart and its conduction system has been studied in several animal species, but there is no express that they represent bundles of Purkinje fibers. A comprehensive research on the ostrich (Struthio camelus) severe u fl orescence after incubation in antisera up to the heart. The results of this survey in future will be used as basic intermediate filament protein skeleton is also backing this knowledge. suggestion [5]. A comparative ultrastructural study of bovine Purkinje fibers and common myocytes during fetal development has 2. Materials and Methods been undertaken by Forsgren and Thornell [ 6]. Differences between the two cell types with respectability 2.1. Light Microscopy. Five hearts from healthy male ostriches to the accommodated disc, amount of myobfi rils, sequence were used. eTh hearts were collected at the slaughter house of mitochondria, amount of glycogen, and formation of T- immediately aeft r slaughter. eTh average weight of the hearts tubules became apparent gradually. In all stages studied, a was 1054.33± 172.34 g; the length of the long axis was 19.33 redundancy of intermediate filaments was typical for the ± 1.05 cm; and the circumferential length at the coronary Purkinje fibers. Myob fi rillar M-bands developed an ear- groove was 35.66± 1.04 cm. Aeft r removal of pericardium, lier stage in Purkinje b fi res than in ordinary myocytes. the hearts were ushe fl d with normal saline and subse- Myofilament-polyribosome complexes typical of adult cow quently immersed in 10% bueff r neutral formalin for 72 hrs Purkinje fibers were not seen in the fetal hearts [ 6]. (ventricular apex was cut off to permit the penetration of The ostrich heart has some different features from the formalin into the lumen). eTh right and left atrium, right other birds. In the ostrich, fibrous pericardium as sternoperi- muscular valve, and interarterial septum were separated and cardial ligament attaches along the thoracic surface of the divided into several segments. Each segment was dehydrated, sternum. eTh central edge of muscular valve hangs down into cleared, and embedded in paraffin. Serial sections of 6–8 Lm International Journal of Zoology 3 (a) (b) Figure 4: (a) Photomicrograph from the microscopic location of the b fi rous white sheet in between the pectinate muscles (PE), in the right atrium (RA) in the male ostrich heart. Green Masson’s Trichrome: CT—connective tissue mass, CO—columns of Purkinje cells. (b) Photomicrograph from the microscopic location of the b fi rous white sheet (WP) and related clauses (arrow) in right atrium the male ostrich heart: RA—right atrium bottom, PE—shoulder muscles. than normal muscle fiber, about 5.5–16 𝜇 m. The arrangement of the component in P-b fi er is different from cardiac muscle fibers. The great part of the fiber is composed of clear, struc- ture less sarcoplasm, and the myofibrils tend to be confined to a thin ring around the periphery of the cells. They have one or more large nuclei centrally located within the b fi er (Figure 1). P-bfi er in the heart of the ostrich was distributed widely. Throughout the endocardial layers, particularly the subendocardial layer, numerous P-fibers, arranged in one or more rows, are seen (Figure 2). In the myocardium, between muscles bundles, the P-fibers are seen. Passing outwards from the network of P-bfi ers lying in the endothelial layer, there are large numbers of conduction b fi er tracts. These tracts Figure 5: Photomicrograph from the microscopic location of the divide up, passing between the muscle fiber bundles, and sinoatrial node (SAN), showing P cells (P), transitional cells (T), and eventually the nes fi t divisions of the tracts, single Purkinje intermediate (I). Arrow—endothelial cells in surface sinuatrial valve bfi ers, are found within the bundles in close association of the sinus venosus, Green Masson’s Trichome. with the muscle be fi rs. eTh se be fi r tracts are usually found in association with the branches of the coronary arteries (Figure 3). The P-fibers are occasionally seen in epicardial layer but occurs lie in protrusion of epicardium below of the thickness were cut, mounted, and stained with H&E and surface of myocardium around coronary arteries. In the right Green Masson’s Trichrome [8]. auricleofthe ostrichheart,P-bfi ers arefound mostextenely beneath the endocardium as a single fibre or well-developed 2.2. Electron Microscopy. Three other hearts were removed tracts.Theselatterare foundmostfrequentlyinthe junction just aer ft slaughter and quickly immersed in Karnovsky’s of auricle with right atrium, and macroscopically they are solution for xfi ation. Cubes of tissue (about 1 mm) were with fibers sheet in this junction ( Figure 4). post-fixed in 1% osmium tetroxide with 0.1 m phosphate eTh conducting system of the heart (sinoatrial node, bueff r. Specimens were dehydrated in ethanol and embedded arterioventricular node his bundle and its branches) consists in epoxy resin. Thin sections (0.5–1 Lm) were stained with of these b fi ers. eTh structure of P-fiber varies according to the toluidine blue to identify the location of AV node. Ultra- part of conducting system in which they occur. eTh sinoatrial thin sections (600A ) were mounted on the copper grids node is composed of P-fibers and intermediate fibers (the and stained with uranyl acetate and lead citrate and were fibers which, in appearance, are intermediate between P- examined with a Philips CM-10 electron microscope, and bfi ersand cardiacmusclefibers). P-bfi ersare locatedinthe electromicrographs were prepared. peripheral region of this node and passing away from it. In the initial stages of their passage away from the node, they have a thick connection tissue sheet (Figure 5). 3. Results The atrioventricular node is composed of fibers which Purkinje fibers in the ostrich heart are large specialized resemble P-b fi er more closely than the myocardial muscle cardiac muscle b fi ers. eTh y have a much greater diameter fibers. Posteriorly, the AV-node narrows down somewhat and 4 International Journal of Zoology CT AVB AVN Figure 8: Photomicrograph from the microscopic location connect- Figure 6: Indicative junction of the arterioventricular node (AVN) ing the left stalk in the connecting area to atrioventricular valve. and arterioventricular bundle (AVB) in the male ostrich heart. CT—connective tissue mass, P—Purkinje cells, E—elastic b fi ers, Green Masson’s Trichrome. F—fibroblast cell, C—collagen fibers, P—parietal wall of the right ventricle; H&E. RA FR AM ∗ MS IV P Figure 7: Photomicrograph from the microscopic location of the Figure 9: The heart of male ostrich, showing the anatomical Purkinje cells( ) in arterioventricular of bundle (AVB) in the male location of the atrioventricular valve. FR—bfi rous ring, RA—right atrium, IV—interventricular septum, M—right muscular valve, ostrich heart. C—collagen b fi ers, arrow—fibroblast; Green Masson’s Trichrome. MS—muscular stalk, AM—connect the left stalk. 4. Discussion continues as the arterioventricular (His) bundle (Figure 6). This bundle itself is composed of a large number of P- The distribution of Purkinje fibers has been studied in various fibers. Three bundle branches (right/left and recurrent) are mammals. In mammals, the Purkinje network is distributed consisting of P-fibers which are arranged as a cord ( Figure 7). in the subendocardial connective tissue in ventricle. es Th e The moderator bands, which are found in the right and networks conduct the cardiac excitation from right and left left ventricle of the ostrich’s heart, consist of only dense his bundle to the myocardium. In human and dogs, the irregular connective tissue, and the Purkinje cells fill the core Purkinje cell in the network is cylindrical or fusiform in shape of moderator bands. There was cell-to-cell communication and arranged in a parallel pattern [9]. In ungulates (sheep and between Purkinje be fi rs within the bundle. eTh Purkinje cells goat), the chain of Purkinje cells was larger than myocytes, were surrounded by connective tissue sheath (Figure 8). and 2–8 oval cells formed these network. The cells connect eTh thick muscular stalk attached the peripheral edge of to each other by desmosomes and gap junction. These cells themuscularrightAVvaluetothearterio-ventricularseptum are covered by a thick sheath of reticular b fi ers [ 10]. In rat and rough parietal wall of the ventricle. Histologically it is and mice, Purkinje cells were very similar to ventricular composed of Purkinje fibers ( Figure 9). myocytes even a little smaller. eTh y are cylindrical in shape With the electron microscopy, the P-cell is easily distin- and organized in parallel pattern, continuing with ventricular guished. The main distinction feature is the lack of electron myocytes in the endocardium [11]. density and having a light appearance, due to the absence of Various aspects of the histochemistry of Purkinje b fi ers organized myofibrils. P-cells usually have two nuclei with a have been studied by Getty [12]and Gossrau[13]. The obser- mass of short, delicate microfilaments scattered randomly in vations of DiDio [14], Hirako [15], and Sommer and Johnson the cytoplasm; they contain short sarcomeres and myofibril- [16] on the general morphology of the ordinary and Purkinje lar insertion plaque. eTh y do not have T-tubules ( Figure 10). cells of the fowl heart have been confirmed. The Purkinje cells International Journal of Zoology 5 (a) (b) Figure 10: (a) Electromicrograph of two P cells (P) represents the folded membrane (arrow), nucleus (N), myofibrils (M), and mitochondrial (Mt). (b) Electromicrograph part of the P cell, showing leptomer (L), along myob fi ril (M). of the fowl are similar in almost all aspects to those of mam- deep into the interventricular septum and then bifurcate mals.They do nothavestep-like intercalated discsbut have into right and left limb. The later branch divides up from irregularly arranged areas of membrane apposition, which the network of P-fibers. Prakash’s [ 19] description does not possess desmosomes, myob fi rillar insertion plaques, and exactly coincide with that of DiDio [14]for thepigeonand large pentalaminar nexuses. No transverse tubular system is swan but resemble more closely to that of Drennan [21]for present, and the sarcoplasmic reticulum is poorly developed. the Ostrich. Similarly, the description of Yousuf [22]for the eTh few myofibrils are irregularly arranged. eTh Purkinje heartofpasserdieff rsinthe basicstructure of this part of the cellshavebeenobservedinthisstudy to containrounded conducting system. aggregations of leptomeres. Leptomeres have previously been One of the features of specific interest in the ostrich heart described by Hirako [15] who suggested that they represented is the presence of moderator bands in both the right and left an aberrant form of muscle bfi ril arising during development. ventricles and in different locations. eTh right ventricle has Thisisunlikelysince they arepresent in almost allPurkinje one tendinous moderator band about the base of the ventricle cells. that extends from the septum to the muscular valve. Also the It seems reasonable to assume that they are associated moderator bands are usually about apex of the right ventricle with myofibrillar formation or destruction since they are seen that extend from septum to parietal wall. In the left ventricle, in association with large masses of disorganized filaments there were some tendinous moderator bands close to the andalsoincontinuitywithapparentlynormalmyobfi rils. apex that extend from septum to parietal wall and between The conducting system consists of the sinoatrial node, the trabeculae carneae of parietal wall. The moderator bands atrioventricular node and bundles, and highly complex net- tend to prevent over distension and serve as the pathway for work of n fi e bundles and tracts [ 16]. Although SA node has the passing of Purkinje fibers across the lumen of the cavity been demonstrated in other birds, there is still some doubt forming a part of the conducting system. Anatomically, the as to its position and even its presence as a discrete node in location of the moderator band in the right and left ventricle birds [17]. Concluded from physiological evidence that an SA of the ostrich heart is different from the other animals. er Th e node was present near the termination of the right precaval were no papillary muscle in the right ventricle of the ostrich vein.Thenodeinanostrich heartiscomposedoffibers, and the moderator band attaches directly to the ventral which in appearance are intermediate between muscle b fi ers surface of muscular valve from interventricular septum. andtruePurkinjefibers.Peripherallywithinthe node and Since in human [23, 24] the moderator band extends passing away from it are several true P-fibers. eTh distribution between interventricular septum and ventricular free wall of P-fibers within the auricles in ostrich heart is similar to and in domestic animals [25]and ungulates[26]these bands that described by Davis [18]for thepigeon. Prakash[19]has extend from interventricular septum to the papillary muscle stated that the atria are devoid of P-be fi rs. In our study, they andthere is no connection to thevulvarcusps.Inthe Ostrich arefound within themyocardiuminassociation with blood left ventricle, despite the presence of papillary muscle, these vessels, and occasionally in the epicardium [20]. Davis [18] bands have no connection to them. Histologic structure of stated that the auricular P-b fi ers stop short at the base of the moderator band showed that they have muscular tissue in auricles and that there are no interconnections between them various proportions with connective and conductive tissue and the reminder of the cardiac conducting system. [27]. It is similartothatofthe human[28], ungulate [26], Intheostrich,theAV-nodeliesinthebaseoftheauricular sheep [24, 29]and goat [24]heartsbut in thecarnivores, septum. It is very close to the junction of the auricular and a real moderator band was never found [26]. Whatever is ventricular septa. It is composed of b fi ers which resemble P- the size and shape, the moderator band must be regarded bfi ersmoreclosely than themyocardialmusclefibres andthat as the shortest pathway from interventricular septum to the they are not identical to those of the SA-node. As Prakash free wall of left and right ventricle in the ostrich and other [19] reported, the atrioventricular bundle in our study extend animals. The Purkinje fibers are large in size and similar in 6 International Journal of Zoology most cellular characteristics in ostrich and dog [30], but in [14] L. J. DiDio, “Myocardial ultrastructure and electrocardiograms of the hummingbird under normal and experimental condi- the ostrich, there is no perinuclear clear area. eTh re is a little tions,” Anatomical Record,vol.159,no. 4, pp.335–352,1967. glycogen in these cells, but in human and mammals these cells [15] R. Hirako, “Fine structure of Purkinje fibers in the chick heart,” arerichinglycogen[4]. The Purkinje fibers are organized Archivum Histologicum Japonicum,vol.27, no.1,pp. 485–499, into the bundle with cell-to-cell communication and little lateral communication. In the ostrich, there is a sheath of [16] J. R. Sommer andE.A.Johnson,“Cardiacmuscle—acompar- connective tissue around the Purkinje cells, but in human and ative ultrastructural study with special reference to frog and mammals there is no b fi rous sheath around these cells [ 25]. chicken hearts,” Zeitschrift f u¨r Zellforschung und Mikroskopische This organization of the bundle fibers increases the spread Anatomie, vol. 98, no. 3, pp. 437–468, 1969. of propagated impulses and inhibits the transverse spread. In [17] E. Mangold and T. Kato, “Zur vergleichenden Physiologie des the right ventricle, there is one musculotendinous moderator ¨ ¨ His’schen Bundels,” Pfl ugers Archiv,vol.160,pp. 91–131,1914. band about the base of the ventricle, which extends from the [18] F. Davis, “eTh conducting system of the bird’s heart,” Journal of interventricular septum to the muscular stalk of the muscular Anatomy,vol.64, pp.129–146,1930. valve. It was single and sometimes branched [4]. [19] R. Prakash, “eTh heart and its conducting system in the common Indian fowl,” Proceedings of the National Institute of Acknowledgment Sciences of India,vol.22, pp.22–27,1956. [20] R. C. Truex, Comparative Anatomy and Functional Consider- eTh authors are grateful to the research council of the Shiraz ation of the Cardiac Conducting System, Elsevier, Amsterdam, University for providing financial assistance. The Netherlands, 1961. [21] M. R. Drennan, “eTh auriculo-ventricular bundle in the bird’s heart,” British Medical Journal,vol.1,pp. 321–322, 1927. References [22] N. Yousuf, “The conducting system of the heart of the house [1] O. 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