Features of presentation of the structure of the human spleen in the course of histology

Authors

  • O.Yu. Pototska
  • K.M. Shevchenko

Keywords:

human spleen, species-specific features, opened blood supply, white pulp, marginal sinus

Abstract

ABSTRACT. Lymphoid organs are characterized by a large number of species-specific features, which depend on the size of the body, the level of physical activity, the nature of the diet and many other factors. Therefore, there are lots of contradictory scientific articles, in which authors compare organs of this system without taking into account the species of the studied animals, or extrapolate the obtained data to humans, which inevitably leads to confusion. Spleen is an important organ of immune system, since it filters blood from foreign antigens, produces antibodies and pro-inflammatory cytokines during systemic inflammatory diseases. There are many controversies about spleen structure in the scientific literature, in particular about the system of its blood supply. Some authors state that spleen has a combination of opened and closed blood capillaries, while others claim that blood circulation in human spleen is completely opened. The presence of marginal sinus as well as perimarginal cavernous sinus in the respective zone of white pulp is also the subject of debate. According to the recent discoveries made with the help of immunocytochemistry and three-dimensional modeling such terms as “periarterial macrophage sheaths" or “vagina periarteriolaris macrophagocytica” and “cords of Billroth” are revised and reconsidered. Another relevant question is the possibility of human spleen to store a reserve portion of blood and to inject it to the bloodstream during the physical activity, stress or after the massive hemorrhage. In this review, we have analyzed species-specific features of human spleen structure and functions to answer all above mentioned controversial questions. Correlations between the innervation and immune processes have also been reviewed.

References

  1. Mesche AL. Junqueira's Basic Histology Text & Atlas (15th ed.). McGraw-Hill Medical; 2018. 562 р. doi: https://doi.org/10.26641/1997-9665.2019.3.101-104
  2. Wojciech P, Ross MH. Histology: A Text and Atlas: With Correlated Cell and Molecular Biology. Eighth Edition. Philadelphia: LWW; 2018. 928 р. doi: https://doi.org/10.26641/1997-9665.2019.4.76-89
  3. Lucyk OD, Chajkovs'kyj JuB, Barіnov EF, Bіlash SM, Bilyj RO, Bobryshheva ІV, Bojchuk TM, Vas'ko LV, Volkov KS, Gerashhenko SB, Djel'cova OІ, Jeroshenko GA, Zaharov AA, Kashhenko SA, Lysachegnkoo OD, Maslovs'kyj S Ju, Mel'nyk NO, Nakonechna OV, Pelypenko LB, Sіlkіna JuV, Stechenko LO, Sokurenko LM, Sulajeva OM, Ul'janov VІ, Shepіt'ko VІ, Shepіt'ko KV, Jashhenko AM. Gistologija. Cytologija. Embri-ologija: nacional'nyj pidruchnyk dlja studentiv vys-hhyh navchal'nyh zakladiv MOZ Ukrai'ny [Histology. Cytology. Embryology: a national textbook for students of higher educational institutions of the Ministry of Health of Ukraine]. Vinnycja: Nova Knyga; 2018. 496 p. Ukrainian.
  4. Afanas'ev JuI, Jurina NA, Aleshin BV, Vinnikov JaA, Katinas GS, Kotovskij EF, Radostina AI. Gistologija, jembriologija, citologija: uchebnik [Histology, embryology, cytology: a textbook]. Moscow: GJeOTAR-Media; 2016. 800 p. Russian.
  5. Ruddle NH. Lymphatic vessels and tertiary lymphoid organs. The Journal of clinical investigation. 2014;124(3):953-959. doi: https://doi.org/10.1172/JCI71611
  6. Prassopoulos P, Daskalogiannaki M, Raissaki M, Hatjidakis A, Gourtsoyiannis N. Determination of normal splenic volume on computed tomography in relation to age, gender and body habitus. Europian Radiology. 1997;7(2):246-248. doi: 10.1007/s003300050145
  7. Hartwig H, Hartwig HG. Structural characteristics of the mammalian spleen indicating storage and release of red blood cells. Aspects of evolutionary and environmental demands. Experientia. 1985;41(2):159-163. doi: 10.1007/BF02002608
  8. Udroiu I. Storage of Blood in the Mamma-lian Spleen: an Evolutionary Perspective. Journal of mammalian evolution. 2017;24(3):243–260. doi: https://doi.org/10.1007/s10914-016-9342-0
  9. Persson S. On blood volume and working capacity in horses. Studies of methodology and physiological and pathological variations. Stockholm: Acta Veterenaria Scandinavica; 1967. 189 p. URL: https://lib.ugent.be/catalog/rug01:002176252
  10. Stewart IB, McKenzie DC. The human spleen during physiological stress. Sports Medicine. 2002; 32(6):361-369. doi: 10.2165/00007256-200232060-00002
  11. Stewart IB, Warburton DE, Hodges AN, Lyster DM, McKenzie DC. Cardiovascular and splenic responses to exercise in humans. Journal of applied physiology. 2003; 94(4):1619-26. doi: 10.1152/japplphysiol.00040.2002
  12. Espersen K, Frandsen H, Lorentzen T, Kan-strup IL, Christensen NJ. The human spleen as an erythrocyte reservoir in diving-related interventions. Journal of applied physiology. 2002; 92(5): 2071-2079. doi: 10.1152/japplphysiol.00055.2001
  13. Katz TC, Singh MK, Degenhardt K, Rivera-Feliciano J, Johnson RL, Epstein JA, Tabin CJ. Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. De-velopmental cell. 2012;22(3):639–650. doi: https://doi.org/10.1016/j.devcel.2012.01.012
  14. Mebius RE. Kraal G. Structure and function of the spleen. Nature Reviews Immunology. 2005; 5(8):606–616. doi: 10.1038/nri1669
  15. Guisado Vasco P, Villar Rodríguez JL, Ibañez Martínez J, González Cámpora R, Galera Davidson H. Immunohistochemical organization patterns of the follicular dendritic cells, myofibroblasts and macrophages in the human spleen--new considerations on the pathological diagnosis of splenectomy pieces. International journal of clinical and experimental pathology. 2009; 3(2):189–202.
  16. Steiniger B, Barth P, Hellinger A. The perifollicular and marginal zones of the human splenic white pulp do fibroblasts guide lymphocyte immigration?. The American journal of pathology. 2001;159(2):501–512. doi: 10.1016/S0002-9440(10)61722-1
  17. Yamamoto K, Arimasa N, Yamamoto T, Tokuyama K, Kobayashi T, Itoshima T. Scanning electron microscopy of the parimarginal cavernous sinus plexus of the human spleen. Scanning electron microscopy. 1979;3(3):763–768.
  18. Schmidt EE, MacDonald IC, Groom AC. Microcirculatory pathways in normal human spleen, demonstrated by scanning electron microscopy of corrosion casts. The American journal of anatomy. 1988;181(3):253–66. doi: 10.1002/aja.1001810304
  19. Steiniger B, Barth P. Microanatomy and Function of the Spleen. Adv Anat. Embryol. Cell. Biol. 2000;151(III-IX):1-101. doi: 10.1007/978-3-642-57088-9. PMID: 10592524
  20. Steiniger B, Barth P, Herbst B, Hartnell A, Crocker PR. The species-specific structure of microanatomical compartments in the human spleen: strongly sialoadhesin-positive macrophages occur in the perifollicular zone, but not in the marginal zone. Immunology. 1997; 92(2):307–316. https://doi.org/10.1046/j.1365-2567.1997.00328.x
  21. Steiniger BS, Ulrich C, Berthold M, Guthe M, Lobachev O. Capillary networks and follicular marginal zones in human spleens. Three-dimensional models based on immunostained serial sections. PLoS One. 2018;13(2):e0191019. doi: 10.1371/journal.pone.0191019.
  22. Blue J, Weiss L. Periarterial macrophage sheaths (ellipsoids) in cat spleen--an electron microscope study. The American journal of anatomy. 1981; 161(2): 115–34. doi: 10.1002/aja.1001610202.
  23. Steiniger BS, Seiler A, Lampp K, Wilhelmi V, Stachniss V. B lymphocyte compartments in the human splenic red pulp: capillary sheaths and periarteriolar regions. Histochemistry and Cell Biology. 2014; 141: 507–518. doi: 10.1007/s00418-013-1172-z
  24. Steiniger BS. Human spleen microanatomy: why mice do not suffice. Immunology. 2015; 145(3):334–46. doi: 10.1111/imm.12469
  25. Steiniger B, Bette M, Schwarzbach H. The open microcirculation in human spleens: a three-dimensional approach. The journal of histochemistry and cytochemistry official journal of the Histochemistry Society. 2011; 59(6):639–648. doi: 10.1369/0022155411408315
  26. Young B, Woodford P, O'Dowd G. Wheater's functional histology: a text and colour atlas. Philadelphia: Elsevier Health Sciences; 2013. 464p. Available from: https://www.elsevier.com/books/wheaters-functional-histology/young/978-0-7020-4747-3
  27. MacDonald IC, Ragan DM, Schmidt EE, Groom AC. Kinetics of red blood cell passage through interendothelial slits into venous sinuses in rat spleen, analyzed by in vivo microscopy. Micro-vasc Res. 1987;33(1):118-34. doi: 10.1016/0026-2862(87)90011-2
  28. Chen LT, Weiss L. The role of the sinus wall in the passage of erythrocytes through the spleen. Blood. 1973;41(4):529-37. doi: 10.1182/blood.V41.4.529.529.
  29. Ultmann JE, Gordon C S. The removal of in vitro damaged erythrocytes from the circulation of normal and splenectomized rats. Blood. 1965; 26(1): 49-62. doi: 10.1182/blood.V26.1.49.49
  30. Schmidt EE, MacDonald IC, Groom AC. Comparative aspects of splenic microcirculatory pathways in mammals: the region bordering the white pulp. Scanning Microsc. 1993;7(2):613-28. Available from: https://api.semanticscholar.org/CorpusID:25460319
  31. Groom AC, MacDonald IC, Schmidt EE. Splenic Microcirculatory Blood Flow and Function with Respect to Red Blood Cells. In: Bowdler A.J. (eds). The Complete Spleen. Humana Press, Totowa, NJ, 2002: 23-50. doi: 10.1007/978-1-59259-124-4_3.
  32. Naito M, Hayashi S, Yoshida H, Nishikawa S, Shultz LD, Takahashi K. Abnormal differentia-tion of tissue macrophage populations in 'osteopetrosis' (op) mice defective in the production of macrophage colony-stimulating factor. Am J Pathol. 1991 Sep;139(3):657-67. Available from: https://www.researchgate.net/publication/21267852_Abnor-mal_differentiation_of_tissue_macrophage_populations_in_'osteopetrosis'_op_mice_defective_in_the_production_of_macrophage_colony-stimulating_factor_M-CSF_or_CSF-1
  33. Vidal S, Tremblay ML, Govoni G, Gauthier S, Sebastiani G, Malo D, Skamene E, Olivier M, Jothy S, Gros P. The Ity/Lsh/Bcg locus: natural re-sistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J Exp Med. 1995;182(3):655-66. doi: 10.1084/jem.182.3.655.
  34. Borges da Silva H, Fonseca R, Pereira RM, Cassado Ados A, Álvarez JM, D'Império Lima MR. Splenic Macrophage Subsets and Their Function during Blood-Borne Infections. Front Immunol. 2015;6:480. doi: 10.3389/fimmu.2015.00480.
  35. Standring S. (Ed.). Gray's Anatomy, 42nd Edition. Edinburgh: Churchill Livingstone/Elsevier; 2020;1606 p. Available from: http://www.clinicalkey.com/dura/browse/bookChapter/3-s2.0-B9780443066849X5001X
  36. Heusermann U, Stutte HJ. Electron Micro-scopic Studies of the Innervation of the Human Spleen. Cell and Tissue Research. 1977;184(2): 225–236. doi:10.1007/BF00223070
  37. Felten DL, Felten SY, Carlson SL, Ol-schowka JA, Livnat S. Noradrenergic and peptider-gic innervation of lymphoid tissue. J Immunol. 1985;135(2 Suppl):755s-765s. Available from: https://www.jimmunol.org/content/135/2/755
  38. Murray K, Reardon C. The cholinergic anti-inflammatory pathway revisited. Neurogastroenterol Motil. 2018;30(3):10.1111/nmo.13288. doi: 10.1111/nmo.13288
  39. Borovikova L, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins L R, Wang H, Abumrad N, Eaton JW, Tracey KJ. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000; 405:458–462. doi: 10.1038/35013070
  40. Guyot M, Simon, T, Panzolini C, Ceppo F, Daoudlarian D, Murris E, Macia E, Abélanet S, Sridhar A, Vervoordeldonk MJ, Glaichenhaus N, Blancou P. Apical splenic nerve electrical stimulation discloses an anti-inflammatory pathway relying on adrenergic and nicotinic receptors in myeloid cells. Brain, behavior, and immunity. 2019; 80:238-246. doi: 10.1016/j.bbi.2019.03.015

Downloads

Published

2023-06-26

How to Cite

Pototska , O. ., & Shevchenko , K. . (2023). Features of presentation of the structure of the human spleen in the course of histology. Морфологія / Morphologia / Morfologìâ, 15(4), 121–129. Retrieved from https://morphology.dma.edu.ua/article/view/282957

Issue

Section

Статті