The Koch’s Triangle Is an Unjustified Eponym: The Building of Triangular Locus of the Atrioventricular Node from Todaro to Tandler

What is known today as Koch’s triangle (the triangle of the atrioventricular node) is delimited by the fibrous attachment of septal tricuspid leaflet, aperture of the coronary sinus and the tendon linking the inferior vena cava valve ( Eustachian) and central fibrous body (Keith, 1906; Koch, 1909; Tandler, 1913; James, 1999; Drenckham, 2004; Stranding, 2016). It was a construct developed by exceptional anatomists. They were Francesco Todaro ( February 14 th, 1839 in Tripi ,Messina ; October 22 nd, 1918 Rome ) , Sunao Tawara (July 5th, 1873 Nakajima, in Aki -Ōita; January 19th,, 1952 Nakatsu) , Ludwig Aschoff (January 10 th , 1866 in Berlin; 24. June 1942 in Freiburg ,Breisgau), Arthur Keith (February 5th, 1866 in Old Machar, Aberdeenshire ;January 7th, 1955 Downe, Kent) and Carl Eduard Walter Koch ( 3rd. Mai 1880 in Dortmund; 21th November 1962 in Gretesch bei Osnabrück) . Julius Tandler ( February 16 1869 in Iglau/Mähren; August 25 1936 in Moscow) gave the name” Dreieck”, (triangle), focusing on Koch’s contributions (Tandler, 1913). Selected refences on the biographies of these scientists are: Francesco Todaro (Ottaviani, 2019), Ludwig Aschoff (Fye, 1999), Sunao Tawara (Suma, 2001; De Almeida et al., 2020; De Almeida, 2023), Arthur Keith (Keith, 1942; Clark, 1955), Walter Koch (James, 1999; Conti, 2011), J Tandler (Kyle and Shampo, 1990).

It is shown how the contributions of all these authors progressed to this important macro and microscopic concept, the locus of atrioventricular node, and why Koch’s triangle is not a fair eponym and should be replaced by a more informative and unbiased term: atrioventricular node triangle or triangular locus of the atrioventricular node. Previously, the late Thomas James (Ottaviani, 2011) have criticized the soundness of this eponym and ,controversially, the utility of the concept (James, 1999). The utility of the concept, the locus of atrioventricular node, since then has been largely confirmed (Mori et al., 2015). However, the criticisms of Thomas James about the soundness of the eponym although right, lacks a clear temporal description of the events culminating in the concept and two important gaps: the contributions of Tawara, not only based in his thesis (Tawara, 1906a, 2000), and Arthur Keith. In particular, the contributions of Arthur Keith on this , so far as I know have not been considered except by a brief mention given in a recent paper (De Almeida, 2023).

The announcement of the Knoten (node) and its place.

In a congress of the German physiological society held in Marburg, 14-16 June of 1905 the Knoten (node) was announced for the first time as a structure confined in the atrial portion of the atrio ventricular bundle (Aschoff, 1905) . Ludwig Aschoff , Tawara’s mentor and then head of the anatomic pathological institute at Marburg, Germany, gave a succinct but clear summary of Tarawa’s, in course, investigation and presented microscopic preparations produced by Tawara (Aschoff, 1905). A significant excerpt from Aschoff’ seminar is selected: “Atrial fibers first appear as a closed bundle at the coronary sinus. They then run anteriorly along the atrial septum to the area of ​​the insertion of the medial tricuspid leaflet, where they form a tangled network and then, together with the plexus from which the fibers of the ventricular segment arise, form the so-called node. This lies as a flat, ridged structure in the fibrous septum between the tricuspid and mitral insertions, and from it the ventricular fibers pass anteriorly through the fibrous septum in an easily traceable bundle to the ventricular septum”(Aschoff, 1905). This communication was published in September 26th in the Muenchener Medizinische wochenscrift ( Munich Medical Weekly) (Aschoff 1905). Tawara himself had produced an account of his almost finished doctoral thesis : ”Die topographie und histologie der brückenfasern “ (The topography and histology of the bridge fibers ) received by the Zentrallblatt fur Physiologie ( key papers in Physiology) in April 17^th 1905 and published at the end of January 1906 (Tawara, 1906b) . That was not a brief communication but a full seven pages paper without illustrations. Tawara anticipated much of the material that would be further developed in his 1906 monography (Tawara, 1906a), which has now an English translation (Tawara, 2000). Tawara stressed in that paper: “So far, I have only been able to identify one center that has been precisely characterized histologically, and which, in my opinion, has its center in a mesh-like node in the atrial septum, directly above the atrioventricular fibrous septum. From this node, a fiber bundle runs backward, often to the anterior border of the coronary sinus, and a second fiber bundle runs anteriorly downward through the atrioventricular fibrous septum, where it continues with the system of Purkinje fibers …”. Tawara mentioned as well that the system is present in birds besides mammals. He particularly stressed that the atrial node is fully irrigated and defined its microscopic aspects: “These fibers are characterized by various features: ...they are narrower than the remaining fibers of the atrial muscle and are very rich in nuclei and exhibit slight fibrillar differentiation, limited only to the peripheral layer. The protoplasm of these fibers always stains a different color than the other muscle fibers. In their imperfect development, they resemble embryonic muscle fibers, but can already be clearly distinguished from the rest of the muscles in the newborn “. Tawara (Tawara, 1906c) , on second half of February , also published the histologic analysis of the Hering’s (Henrich Ewald Hering (May 3rd, 1866 Vienna; December 16th, 1948 Papenhusen)) material on the bundle transection (Hering, 1905; Tawara, 1906c) (Figure 1). In this publication he depicted the position of the node and the bundle. These would be further improved in his monography. Previously, Hering (Hering, 1905) had provided macroscopic photographs illustrating in the real hearts where the bundle should be sectioned to produce atrio- ventricular dissociation ( Figure 2)

James Mackenzie (April 12th, 1853 Pictonhill Scone; January 25th, 1925 London) at Burnley read the Aschoff’s report (Aschoff, 1905) and communicated it to Arthur Keith who was struggling without success to reproduce His junior’s (His, 1949) (Wilhelm His Jr (December 29th,1863 Basel; November 10th, 1934 Brombach- Lörrach)) and Hering’s (Hering, 1905) results on the atrioventricular bundle. Arthur Keith afterwards sent in February 3rd 1906 a letter to The Lancet that was published in March 3^rd 1906 (Keith, 1906) . Keith exposed that he was indeed preparing a previous letter to The Lancet denying the existence of the bundle: “There may be an error in my observation or in my technique. I simply draw attention to the fact that I have failed to find a muscular bundle in the position described by His and Hering and that before it is accepted as the anatomical basis of Stokes-Adams disease its constancy must be proved. At least it is well to have the existence of the bundle of His verified at the very commencement, so that it may not have a circulation of two centuries before it is called in as false coin. Some days after writing the part of this letter given above Dr. James Mackenzie sent me a cutting from the Muenchner Medizinische Wochenschrift of Sept. 26th, 1905 p. 1904, in which Dr. L. Aschoff gave an account " Ueber die Untersuchungen des Herrn Dr. Tawara, die Bruckenfasern betreffend und Demonstration der zugehorigen mikroskopischen Praparate” (On the investigations of Dr. Tawara, concerning the bridge fibers and demonstration of the associated microscopic preparations) ….With this account to guide me I renewed my search with success” (Keith, 1906) .

It is worthy to recognize that Keith, although reading the description of the node by Aschoff (Aschoff, 1905) overlooked the description of the “Knoten” in his letter , apparently he was more focused in identify the atrioventricular bridging fibers of the atrioventricular bundle (His bundle). Confirming that he wrote ” since it is probable that others may find the initial difficulty I experienced in dealing with this intricate region of the heart I propose to give briefly by the aid of a diagram some of the points which have proved most useful to me”(Figure 3 A). This diagram, as mentioned (De Almeida, 2023), is a first description of the landmarks delimiting in the atrial side a triangular area ( red dotted lines in Figure.3) whose components are known today as Koch’s triangle. Unfortunately, Keith not portrayed the Knoten (node) described by Aschoff’s communication, but only the atrioventricular bundle as described by Aschoff. However, he described the fibrous tendon linking inferior vena cava valve (Eustachian) to central fibrous body as a novelty:” In the musculature beneath the endocardium will be found two fibrous bands (see g, h, in Figureure) which are of great interest but, so far as I know, have never been described. These bands begins in the membranous space and run through the musculature of the septum to the Eustachian (g) and Thebesian (h)…”(Keith, 1906) . Keith was unaware that Francesco Todaro (Todaro, 1895) had described the fibrous structure arising from vena cava inferior valve (Eustachian valve) in 1895 (Figure 4). Todaro’s description is more complete than that of Keith: “I immediately noticed that from the right posterior portal/part of the tendinous center, a fibrous ribbon started; and, having followed it, with great care, among the muscular fibers below, I accompanied it up to the posterior pillar of the oval fossa, from where I made sure that it entered through the posterior horn, which originates here, in the Eustachian valve, following it along its entire free margin. I have confirmed this observation later, in many other cases; and I have always found the tendon constant, even when the Eustachian valve is almost deficient ”(Todaro, 1895). Keith described too the nodal artery: “A large artery (with a caliber of 1 to 1. 5 millimeters) invariably perforates the central fibrous body just behind the bundle ; the artery is always bigger than the muscular bundle at the point of perforation”(Keith, 1906). Nevertheless, Keith described, inside the triangular area, a component which is not today mentioned in the triangular locus of the atrioventricular node: a separate tendon arising from coronary sinus valve. Keith, however could be describing a case with a double Tendon as reported previously (James, 1999).

It is almost certain that Keith read also the Tawara’s paper (Tawara, 1906b) because one description is not present in Aschoff’s paper (Aschoff, 1905). He mentioned in the letter to The Lancet” … as Tawara described, fine, multinucleated cells with indistinct striation; I observed also, as he did, that the fibers were accompanied by numerous nerve fibers, and there are cells, too, which have the appearance of ganglionic nerve cells”. The Keith intention was to give a more didactic presentation of Tawara discoveries. He achieved that but neglected the Knoten(node), on the other side he was the first to add the tendon of inferior vena cava in this area as a useful delimitation (Keith, 1906).

Tawara’s monography “Das Reizleitungssystem des Säugetierherzens. Eine anatomisch-histologische Studie über das Atrioventrikular bündel und die Purkinjeschen Fäden“ (Tawara, 1906a) ( The conduction system of the mammalian heart. An anatomical-histological study of the atrioventricular bundle and Purkinje's fibers.(Tawara, 2000) ) was finished December 24^th 1905 at Marburg and published at the beginning of 1906. The Aschoff’s preface was written in March 19^th. In that monography he further developed what was announced before by his Mentor and by himself. Tawara first described the node (knoten) in a human heart (No. 136. The two-year-old child heart). The description is given in the section “Topography of the Atrioventricular Connecting System”. Tawara had previously examined ten dog hearts in which an atrial segment of the connecting system is described, a description compatible with the node. The word knoten (node), however, was not mentioned in these dogs’ hearts descriptions but he had drawn it ( dog heart no 166, Figure3 ) Figure 7A. In consequence, Tawara crystalized the concept of the node (Knoten) just when he studied the human heart No 136 (Figure 5); “By examining the staged microscopic sections, a peculiar muscle group is observed in section No. 105, which is entirely different from the atrial musculature in terms of abundancy and form of nuclei as well as in the arrangement of the muscle fibers. The muscle group is located about 1.5 mm below the lowest attachment of the noncoronary aortic leaflet, in other words, at the infero posterior margin of the membranous septum. It adheres to the atrioventricular fibrous septum (s), i.e. to the origin of the aorta. When compared with the adjacent atrial muscle fibers, the fibers are much smaller and less differentiated. The arrangement is extremely irregular, giving the appearance of a complicated glomerulation - I call this site “the node*” (k). In the following sections, this bundle becomes gradually thicker and extends anteriorly. Consequently, the tip of the bundle protrudes into the fibrous septum (section No. 110). When projected to the left endocardial surface, the extension of the bundle occupies the posterior three quarters of the noncoronary aortic leaflet. The muscle fibers connect with the adjacent ordinary atrial muscle fibers (v) posteriorly and at the right hand margin of the node (Figure. 1 = section No. 110.) (Tawara, 2000). Tawara monography provided drawings helping the macroscopic and microscopic localization of the Knoten (Atrioventricular node). (Figure 1A, B; Figure.6A, B) Tawara macroscopic Figureures show the evident relation of the node with the septal tricuspid leaflet and mitral aortic leaflet, coronary sinus ostium, commissure of septal and antero superior tricuspid leaflet, right and non-coronary leaflets, central fibrous body and membranous septum (Figure 1; Figure 6A, B). The inferior vena cava tendon (Todaro’s tendon), however, is not described or mentioned. In some of his histological Figureures he sketched the tendon but he did not make reference to it . Tawara clearly represented the tendon in Figure 120 plate 1. in a dog heart (Figure 7A). and possibly in Figure 139 in a human heart. (Figure 7B). In general, the upper border of the other Figureures are too close to the fibrous skeleton to see the tendon in different cut levels. However, his descriptions, and Figureures of the node and its relation with surroundings structures are completely original and precise. Shortly, Tawara was the first to describe all components of the triangular locus in its relation with the node excluding the inferior vena cava valve tendon. Koch (Koch, 1909)) as Keith described the tendon of vena cava and assembled it with the other structures previously described by Tawara, constructing the triangle . Koch emphasized the presence of the node and atrioventricular bundle in a Figureure whose main objective was to show the advances he obtained in morphology of sinoatrial node (Koch, 1909; Keith and Mackenzie, 1910)( Figure .8) .Indeed, the main objective of the whole paper was to detail his findings in sinoatrial node and discuss its probable function (Koch, 1909) . He wrote “On the other hand, at another location in the entry of the atrial cavity, more anteriorly near the upper border of the right atrial appendage, there is a peculiar muscular system discovered by Keith and described in more detail by me in a previously published work, which in many respects can be considered parallel to the atrial part of the conduction system between the atrium and the ventricle. I was able to demonstrate it at the time, at the border between the atrium and the cava in the sulcus already discussed, beginning approximately at the upper edge of the atrial appendage. As recent observations have shown me, it appears to extend along the sulcus, its fibers extending outward and downward almost 1 cm further than I previously stated (2 cm) (Figure. 3), where it splits and disappears upward into the musculature of the cava and downward into the atrial musculature…. I consider the demonstration of this muscular system discovered by Keith to be not unimportant, since with a better understanding of its function, disturbances in it may perhaps be able to be used to explain physiological and pathological cardiac processes.”

Dreieck ( triangle ) is not mentioned nor in this paper neither in his magnum opus (Koch, 1922). Koch did not gave credit to Keith, on this particular aspect, who just emphasized the fibers of the atrial portion of the bundle inside of the triangular locus. Both did not gave credit to Todaro (Todaro, 1895) .Both did not stress or write that they were delimiting a triangular area . Tandler (Tandler, 1913) named for the first time the locus as a Koch’s Dreieck ( triangle) (James, 1999)”:Topographically, the nodule was described almost entirely consistently by all authors, although the relationship to the aortic valves was particularly emphasized. This relationship, at least for locating the nodule, does not seem particularly well chosen, since the nodule is most easily located from the right side of the atrial septum. Koch relocated the nodule into the triangle he described. Koch outlined this triangle as follows: The caudal border is formed by the insertion of the tricuspid artery, the calcaneal border by a fold that forms when the junction of the Eustachian and Thebesian valves is tensed to the right with forceps. The fold then runs obliquely forward and downward toward the membranous septum. In my opinion, it is the expression of the tension of Todaro's tendon, which has already been described elsewhere. The posterior border of this triangular field is represented by the orifice of the coronary sinus. Near the apex of this triangle, as Koch quite rightly points out, lies the node. We already emphasized elsewhere that Koch's deductions, as if this field were originally a sensory area, are not valid for evolutionary reasons. However, Koch's topographical definition is certainly acceptable.”. Tandler forgot also that Tawara had described the main relations of the node in right atrial side.

The author did not intended to be exhaustive or dogmatic in matters of the priority of the discoveries. As exposed here Keith and Koch have rediscovered the findings of Todaro and we cannot affirm with absolute certainty that Todaro was the first to describe the tendon of the inferior vena cava valve. These does not invalidate the thesis: to know, that the triangular locus of the atrioventricular node was a collective construct. To prove it we just need one clear and logical sequence of temporally sound events as shown here.

In summary the triangular locus of the atrioventricular node was a collective construct as the majority of human scientific endeavors(Ogden, 2007; Woywodt and Matteson, 2007).

Conflict of interest: There is no conflict of interest.

Acknowledgments: Many thanks to the librarians of Free University of Berlin who gently sent me the paper of Koch W (1909) Weiter Mitteilungen über den Sinusknoten des Herzens. . Verh Deutscth Ges Pathol 13:85–92

Declaration: the author have used as an auxiliary tool for the translation of German original texts , in print and online German-English dictionaries as well as Google translator.

Copyrights: The Figureures shown in this article are free of copyrights.

Ethical issues: The ethical issues are not involved in this article whose main novelty is a revision of an historical error, an eponym widely used in cardiac anatomy.