Abstract
The His bundle is a part of the specialized electrical conduction system that provides a connection between the atrial and ventricular myocardial compartments in both normal and abnormal hearts. The aim of this study was to perform a morphometric analysis of His bundle characteristics of in humans, dogs, horses and pigs and compare them in these studied species. Histological sections of 5 μm thickness were obtained and stained with hematoxylin–eosin and Masson's trichrome; the desmin and periodic acid–Schiff methods were also used for precise identification of cells. The His bundle was found to be longer in horses (2.85 ± 1.02 mm) and pigs (1.77 ± 0.9 mm) than in dogs (1.53 ± 0.8 mm) or humans, in which it was shortest (1.06 ± 0.6 mm). The area and diameters in His bundle cells, were significantly larger in pigs and horses than in humans (p < 0.001) or dogs (p < 0.001). We found two organizational patterns of His bundle components: group I, with large cells and a high amount of collagen fibers in ungulates (pigs and horses); and group II, with smaller cells and lower abundance of collagen fibers in humans and dogs. Documenting cell size variations in the His bundle allows us not only to identify this bundle by histological or anatomical location but also to differentiate these cells from others such as nodal or Purkinje cells. Our analysis revealed that His bundle cells have discrete identities based on their morphometric and histological characteristics.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets in this study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Aouadi S, Mbarki W, Zemzem N (2019) Towards the modeling of the Purkinje/myocardium coupled problem: a well-posedness analysis. J Comput Appl Math 351:136–152. https://doi.org/10.1016/j.cam.2018.10.024
Bharati S, Levine M, Huang SKS, Handler B, Parr GV, Bauerfeind R, Lev M (1991) The conduction system of the swine heart. Chest 100:207–212. https://doi.org/10.1378/chest.100.1.207
Bishop SP, Cole CR (1967) Morphology of the specialized conducting tissue in the atria of the equine heart. Anat Rec 158:401–416. https://doi.org/10.1002/ar.1091580405
Cabrera JA, Anderson RH, Macías Y, Nevado-Medina J, Porta-Sánchez A, Rubio JM, Sánchez-Quintana D (2020) Variable arrangement of the atrioventricular conduction axis within the triangle of Koch: implications for permanent His bundle pacing. JACC Clin Electrophysiol 6:362–377. https://doi.org/10.1016/j.jacep.2019.12.004
De Almeida MC, Sánchez-Quintana D, Davis N, Charles FR, Chikweto A, Sylvester W, Loukas M, Anderson RH (2020) The Ox atrioventricular conduction axis compared to human in relation to the original investigation of Sunao Tawara. Clin Anat 33:383–393. https://doi.org/10.1002/ca.23524
Duan D, Yu S, Cui Y, Li C (2017) Morphological study of the atrioventricular conduction system and Purkinje fibers in yak. J Morphol 278:975–986. https://doi.org/10.1002/jmor.20691
Eliška O (2006) Purkynje fibers of the heart conduction system – history and the present time. Cas Lek Cesk 145:329–335 (PMID: 16639936)
Eriksson A, Thornell LE, Torgny S (1979) Skeletin immunoreactivity in heart Purkinje fibers from several species. J Histochem Cytochem 27:1604–1609. https://doi.org/10.1177/27.12.391995
Forsgren S, Eriksson A, Kjörell U, Thornell LE (1982) The conduction system in the human heart at midgestation – immunohistochemical demonstration of the intermediate filament protein skeleton. Histochemistry 75:43–52. https://doi.org/10.1007/BF00492532
Fuchs E, Weber K (1994) Intermediate filaments: structure, dynamics, function and disease. Annu Rev Biochem 63:345–382. https://doi.org/10.1146/annurev.bi.63.070194.002021
Gianni C, Burkhardt JD, Trivedi C, Mohanty S, Natale A (2018) The role of the Purkinje network in premature ventricular complex-triggered ventricular fibrillation. J Interv Card Electrophysiol 52:375–383. https://doi.org/10.1007/s10840-018-0402-7
Glomset DJ, Glomset ATA (1940) A Morphologic study of the cardiac conduction system in ungulates, dog and man. Part II: the Purkinje system. Am Heart J 20:677–701. https://doi.org/10.1016/S0002-8703(40)90530-0
Ho SY, Kilpatrick L, Kanal T, Germroth PG, Thompson RP, Anderson RH (1995) The architecture of the atrioventricular conduction axis in dog compared to man: its significance to ablation of the atrioventricular nodal approaches. Cardiovasc Electrophysiol 6:26–39. https://doi.org/10.1111/j.1540-8167.1995.tb00754.x
James TN (1970) Cardiac conduction system: fetal and postnatal development. Am J Cardiol 25:213–226. https://doi.org/10.1016/0002-9149(70)90581-3
James TN, Sherf L (1971) Fine structure of the His bundle. Circulation 44:9–28. https://doi.org/10.1161/01.cir.44.1.9
James TN (2002) Structure and function of the sinus node, AV node and Hiss bundle of the human heart: part I – structure. Prog Cardiovasc Dis 45:235–267. https://doi.org/10.1053/pcad.2002.130388
Kawashima T, Sasaki H (2011) Gross anatomy of the human cardiac conduction system with comparative morphological and developmental implications for human application. Ann Anat 193:1–12. https://doi.org/10.1016/j.aanat.2010.11.002
Kistin AD (1949) Observations on the anatomy of the atrioventricular bundle (bundle of His) and the question of the other muscular atrioventricular connections in normal human hearts. Am Heart J 37:849–867
Li J, Logantha SJ, Yanni J, Cai X, Dobrzynski H, Hart G, Boyett MR (2015) From the Purkinje fibers to the ventricle: one dimensional computer simulation for the healthy and failing heart. Conf Proc IEEE Eng Med Biol Soc 2015:34–37. https://doi.org/10.1109/EMBC.2015.7318294
Lowery J, Kuczmarski ER, Hermann H, Goldman RD (2015) Intermediate filaments play a pivotal role in regulating cell architecture and function. J Biol Chem 290:17145–17153. https://doi.org/10.1074/jbc.R115.640359
Mettam RW (1928) The atrioventricular system of the equine heart. Dept. of Agriculture. Onderstepoort, Union of South Africa, pp 745–752
Montoya JA, Ynaraja E (1992) Cardiac arrhythmias in the dog and cat clinic. A bibliographic review and its practical approach. Clin Vet Peq Anim 12:201–228
Nabipur A (2004) Anatomy and histology of the atrioventricular node in the heart of guinea pig (Cavia percellus). Iran J Vet Res 5:204–209
Paulin D, Li Z (2004) Desmin: a major intermediate filament protein essential for the structural integrity and function of muscle. Exp Cell Res 301:1–7. https://doi.org/10.1016/j.yexcr.2004.08.004
Randhawa A, Gupta T, Aggarwal A, Sahni D, Singh RS (2017) Histological topography of the atrioventricular node and its extensions in relation to the cardiothoracic surgical landmarks in normal human hearts. Cardiovasc Pathol 30:38–44. https://doi.org/10.1016/j.carpath.2017.06.005
Shimada T, Arita A (1996) Heart conduction system and accessory pathways. Nippon Rinsho 54:2029–2034
Tawara S (1906) Das Reizleitungssystem des Säugetierherzens; eine anatomisch-histologische Studie über das Atrioventrikularbündel und die Purkinjeschen Fäden. Gustatav Fischer, Jena, pp 114–156
Guyton AC, Hall JE (2006) Texbook of Medical Physiology, eleventh. Elsevier Saunders, Philadelphia, pp 123–124
Tawara S (2000) The conduction system of the mammalian heart: An anatomico-histological study of the atrioventricular bundle and the Purkinje fibers, 1st English Ed. Imperial College Press, London, pp 115–160
Truex RC, Smythe MQ (1965) Comparative morphology of the cardiac conduction tissue in animals. Ann N Y Acad Sci 127:19–33. https://doi.org/10.1111/j.1749-6632.1965.tb49390.x
Uhley HN, Rivkin L (1960) Peripheral distribution of the canine AV conduction system; observations on gross morphology. Am J Cardiol 5:688–691. https://doi.org/10.1016/0002-9149(60)90137-5
Vigmond EJ, Stuyvers BD (2016) Modeling our understanding of the His-Purkinje system. Prog Biophys Mol Biol 120:179–188. https://doi.org/10.1016/j.pbiomolbio.2015.12.013
Waller B, Gering LE, Branyas NA, Slack JD (1993) Anatomy, histology, and pathology of the cardiac conduction system: part II. Clin Cardiol 16:347–352. https://doi.org/10.1002/clc.4960160410
Yoshimura A, Yamaguchi T, Kawazato H, Takahashi N, Shimada T (2014) Immuno-histochemistry and three-dimensional architecture of the intermediate filaments in Purkinje cells in mammalian hearts. Med Mol Morphol 47:233–239. https://doi.org/10.1007/s00795-014-0069-9
Acknowledgements
We thank the Institute of Legal Medicine and Forensic Sciences and the Vijagual Refrigerating Plan in the city of Bucaramanga, Colombia, for donating the specimens studied in this research.
Funding
This work was supported by the “Instituto de Salud Carlos III” and co-funded by “FEDER, “Una manera de hacer Europa” (grant numbers PI19/00246, PI19/00245).
Author information
Authors and Affiliations
Contributions
FGT and ARS conceived and designed the study. FGT performed the experiments. FGT wrote the first draft of the manuscript. FGT and ARS revised the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
The authors declare that all experiment protocols were approved by the Ethics Committee of Universidad Cooperativa de Colombia (No. 014-2018) and comply with resolution 008430 of 1993, decree 2164 of 1992 and Law 10 of 1990 of the local Ministry of Health and with the principles of the Declaration of Helsinki. Additionally, they comply with National Law 84 of 1989, which corresponds to the "National Statute for the Protection of Animals", in Chapter VI of the use of animals in experiments and research.
Consent to participate
Not applicable.
Consent for publication
All authors give consent for publication.
Conflict of Interest
The authors declare that they have no conflict of interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gómez-Torres, F., Ruíz-Sauri, A. Morphometric analysis of the His bundle (atrioventricular fascicle) in humans and other animal species. Histological and immunohistochemical study. Vet Res Commun 45, 319–327 (2021). https://doi.org/10.1007/s11259-021-09812-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-021-09812-4