Anatomy of the inferior pyramidal space tendon in the fetal and neonatal heart: a pilot study

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Abstract

BACKGROUND: Knowing the anatomical features of the inferior pyramidal space tendon of the fetal and neonatal heart (the tendon of Todaro, TT) is important for perinatal cardiac surgery (e.g., with access to the left atrium), but has been virtually unstudied.

AIM: The aim of the study was to evaluate the possibility of dissecting and evaluating the TT macromicroscopically and to obtain preliminary data on its presence, shape, size, branching and local topography in the fetal and neonatal heart.

MATERIALS AND METHODS: Fifteen samples of normal human hearts at 16–40 weeks of gestation were examined. Ten hearts were dissected under an Olympus SZX2-ZB10 microscope (Olympus, Japan) at a magnification ranging from 6.3 to 30×. The length and width of the TT were measured using a Levenhuk M1000 PLUS camera (Levenhuk, Russia) with a resolution of 10 Mpx and Levenhuk lite software. The arithmetic mean, standard deviation, median, extreme values, coefficient of variation and Spearman correlation coefficient (Rs) were calculated. Histologic sections were prepared from five hearts and stained using the Masson trichrome technique.

RESULTS: The TT was detected in all specimens and was always located in the intramyocardial space and/or in the loose connective tissue of the inferior pyramidal space. In all cases, the TT was originated from the right fibrous triangle, anterior to and above the atrioventricular bundle and node, where the TT was most monolithic. The TT then followed between the inferior border of the patent foramen ovale and the opening of the coronary sinus, ending at the valve of the inferior vena cava. In 6 out of 10 cases, the TT had no branches. In 4 out of 10 cases, it divided into two branches covering the opening of the coronary sinus. The TT fibers reaching the right coronary artery were dissected in one specimen. The median width of the TT at the inferior vena cava valve (0.35 mm) correlated with its length (4.63 mm; Rs = 0.821; p = 0.023) and width at the origin (0.24 mm; Rs = 0.929; p = 0.0003).

CONCLUSIONS: The inferior pyramidal space tendon of the heart in the late prenatal and perinatal period of human development is characterized by variable anatomy and constant topography. Variable structure is manifested by variations in tendon branching, a wide range of lengths and especially widths. Constant topography means that the tendon originates, runs, and ends in the same places. This tendon can be identified in fetal and neonatal hearts using macromicroscopic dissection.

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About the authors

Andrey A. Yakimov

Ural State Medical University; Ural Federal University

Author for correspondence.
Email: ayakimov07@mail.ru
ORCID iD: 0000-0001-8267-2895
SPIN-code: 8618-2991

MD, Cand. Sci. (Medicine), Associate Professor

Russian Federation, Ekaterinburg; Ekaterinburg

Eugenia G. Dmitrieva

Ural State Medical University; Ural Federal University

Email: anmayak@mail.ru
ORCID iD: 0000-0002-2973-3481
SPIN-code: 7966-8133
Russian Federation, Ekaterinburg; Ekaterinburg

Anton A. Gaponov

Ural State Medical University; Ural Federal University

Email: gagaponov@gmail.com
ORCID iD: 0000-0002-6681-7537
SPIN-code: 2841-6740
Russian Federation, Ekaterinburg; Ekaterinburg

References

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2. Fig. 1. Todaro tendon (1), surrounded by the myocardium of the right atrium (2), adjacent to the coronary sinus (3) in the inferior pyramidal space. Transverse section. Specimen 275, fetus of 20-21 weeks. Trichrome Masson staining; lens ×40

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3. Fig. 2. The beginning of the inferior pyramidal space tendon from the right fibrous triangle: a — ×4; b — rectangle area from the Fig. a, ×40. Specimen 412, fetus of 16 weeks. 1 — aorta, 2 — left atrium, 3 — right atrium, 4 — bottom of the inferior pyramidal space, 5 — right fibrous triangle, 6 — bundle of His, penetrating part. Trichrome Masson staining

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4. Fig. 3. Variants of the Todaro tendon: a — trunk-line (specimen 298, fetus of 29–30 weeks); b — dichotomous (specimen 507, newborn, 40 weeks); c — trunk-line variant with the anterior elongation (specimen 517, newborn, 36 weeks); d — dichotomous (specimen 489, newborn, 39 weeks). 1 — tendon of Todaro, 2 — valve of the inferior vena cava, 3 — right fibrous triangle, 4 — right fibrous ring, right (5) and left (6) atrioventricular orifices, 7 — aortic root, left atrial (8) and the right (9) atrial wall of the inferior pyramidal space (view from this space), 10 — the coronary sinus opening. The white arrows show the tissue of the atrioventricular node (b, c). The white contour arrows show the penetrating part of the His bundle where the latter passes through the right fibrous triangle (d). The asterisk indicates the posterior branch of the tendon of Todaro (b, d); c — tendon of Todaro exhibits the anterior continuation (*) into the adventitia of the right coronary artery (**). Mesoscopic dissection by means stereoscopic microscope; zoom system: ×0,8 (c), ×1 (а, b, d). Illumination with oblique incident light from an incandescent lamp (а), a ring LED illuminator (b, c, d)

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5. Fig. 4. Posteroinferior parts of the atrial medial walls (walls of the inferior pyramidal space). Specimen 282, fetus of 19 weeks. 1 — Todaro tendon branching at the base of the inferior pyramidal space, 2 — connective tissue at the valve of the inferior vena cava, 3 — cardiac coronary sinus. Masson trichrome staining; lens ×4

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6. Fig. 5. Size distribution of the inferior pyramidal space tendon (histograms) and the relationships between them. Д marks the length of the tendon, Ш (н) means the width of the tendon at the point of origin from the right fibrous triangle, Ш (к) is the width of the tendon at the point of ending at the valve of the inferior vena cava

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