The Open Microcirculation in Human Spleens

Abstract

It has long been debated whether the red pulp of human spleens harbors an open or a closed microcirculation or both. To solve this issue, the authors differentially stained the endothelium in red pulp arterial microvessels and in venous sinuses using brightfield and fluorescence immunohistology with reagents against CD34 and CD141. Three-dimensional models of red pulp arterial microvessels and sinuses were derived from serial double-stained paraffin sections with the help of license-free open-access software. In each model, arterial microvascular ends were traced and verified by reference to the original serial sections. In total, 142 ends were analyzed in the specimens of three individuals. None of these ends was connected to a sinus, suggesting that the human splenic red pulp harbors an entirely open circulatory system. Thus, the spleen is the only human organ where blood passes through spaces not lined by endothelia or other barrier-forming cells.

<b>Three-dimensional reconstruction of serial sections for analysis of the microvasculature of the white pulp and the marginal zone in the human </b><b>spleen </b>

“…However, a 3D reconstruction of the serial sections is a powerful tool that can be used to investigate the splenic microvasculature, because it can provide a 3D conception of the vessels and their surrounding structures. Indeed, this technique was previously applied to an analysis of the branching pattern of the central artery, as well as to a demonstration of the open microcirculation in the human spleen (11,16). In the present study, we performed 3D reconstructions of the vasculature and the white pulp in the human spleen using CD34 immunostained sections.…”

“…SEM of vascular corrosion casts of the human spleen (7) has further confirmed that some of the penicillar arteries, after passing through a splenic follicle, make a hairpin turn and return to the follicle to form bundler arteries. Immunohistochemical studies have focused on the vasculature of the human spleen (11)(12)(13)(14)(15)(16)(17)(18)(19). Steiniger et al performed double staining of serial sections of human spleens for CD34 (a marker for the vascular endothelium) and CD141 (a marker for the sinus en-oxidase activity.…”

“…They further performed a three-dimensional (3D) reconstruction of serial sections immunostained for lymphocyte makers and CD34, and found that the central artery gave off pulp arteries in the vicinity of the splenic follicle (16). A 3D reconstruction of serial sections immunostained for CD34 and CD141 also showed that most of the arterial capillary ends had no connection to the surrounding sinuses in the human spleen (11). Despite these studies of the human splenic vasculature, descriptions of the microvasculature of the white pulp as well as the marginal zone remain highly controversial.…”

Heterogeneity of stromal cells in the human splenic white pulp. Fibroblastic reticulum cells, follicular dendritic cells and a third superficial stromal cell type

“…An additional interpretation of the phenomenon is that splenectomy removes the decisive recirculation compartment, which maintains MZ B‐cell vitality and function. MZ B‐cell survival may depend on bacterial or viral components that are directly extracted from the blood, because the human spleen most likely has an entirely open microcirculation . This means, that capillaries of the human splenic red pulp do not join the venous sinuses, but pour their blood into the loose connective tissue of the splenic cords through open ends.…”

First experience with single incision laparoscopic surgery in Slovakia: Concomitant cholecystectomy and splenectomy in an 11-year-old girl with hereditary spherocytosis

“…The blood elements with undisturbed elasticity of cell membrane subsequently return to the blood circulation by penetrating through the small openings in the walls of specialized capillaries (splenic venous sinuses) (ref. [7][8][9][10] ). The altered erythrocytes in hereditary spherocytosis are vulnerable to splenic sequestration and subsequent lysis and cause the characteristics of this disease such as jaundice, anemia, splenomegaly, and cholelithiasis.…”