Lymphatic system of the eye

Borodin Yu.I.

Research Institute of Clinical and Experimental Lymphology, 2 Timakova St., Novosibirsk, Russian Federation, 630060

Bgatova N.P.

Research Institute of Clinical and Experimental Lymphology, 2 Timakova St., Novosibirsk, Russian Federation, 630060

Nogovitsina S.R.

Research Institute of Clinical and Experimental Lymphology, 2 Timakova St., Novosibirsk, Russian Federation, 630060

Trunov A.N.

Research Institute of Experimental and Clinical Medicine, Novosibirsk, Russia

Konenkov V.I.

NII klinicheskoĭ i éksperimental'noĭ limfologii Sibirskogo otdeleniia RAMN, Novosibirsk

Chernykh V.V.

Novosibirsk branch of the Academician S.N. Fyodorov IRTC «Eye Microsurgery», Ministry of Health of the Russian Federation, 10 Kolkhidskaya St., Novosibirsk, Russian Federation, 630096

Lymphatic system of the eye

Authors:

Borodin Yu.I., Bgatova N.P., Nogovitsina S.R., Trunov A.N., Konenkov V.I., Chernykh V.V.

More about the authors

Journal: Russian Annals of Ophthalmology. 2018;134(2): 86‑91

DOI: 10.17116/oftalma2018134286-90

Read: 8023 times

Download PDF (RU)

Contact the author

Table of contents

To cite this article:

Borodin YuI, Bgatova NP, Nogovitsina SR, Trunov AN, Konenkov VI, Chernykh VV. Lymphatic system of the eye. Russian Annals of Ophthalmology. 2018;134(2):86‑91. (In Russ.)
https://doi.org/10.17116/oftalma2018134286-90

Подписка 2025-2 (Russian Annals of Ophthalmology)

Использование инфографики авторами научных работ

Close metadata

Existence of lymphatic outflow of intraocular fluid is still an open question. Identification of the lymphatic capillaries and vessels in various human organs in normal and pathological conditions became possible with discovery of endotheliocyte markers for lymphatic vessels. However, the available information on the presence of lymphatic structures in the human eye is inconsistent and uncertain. The data on lymphatic drainage of the eye is of interest, particularly because it may help understand glaucoma pathogenesis, mechanisms of development of eye inflammatory diseases, and develop pathogenetic therapies. The article reviews literature and presents the authors’ own views on lymphatic drainage of the human eye.

Keywords:

lymphatic drainage

lymphatic channels

lymphatic region of the human eye

Authors:

Borodin Yu.I.

Research Institute of Clinical and Experimental Lymphology, 2 Timakova St., Novosibirsk, Russian Federation, 630060

Bgatova N.P.

Research Institute of Clinical and Experimental Lymphology, 2 Timakova St., Novosibirsk, Russian Federation, 630060

Nogovitsina S.R.

Research Institute of Clinical and Experimental Lymphology, 2 Timakova St., Novosibirsk, Russian Federation, 630060

Trunov A.N.

Research Institute of Experimental and Clinical Medicine, Novosibirsk, Russia

Konenkov V.I.

NII klinicheskoĭ i éksperimental'noĭ limfologii Sibirskogo otdeleniia RAMN, Novosibirsk

Chernykh V.V.

Novosibirsk branch of the Academician S.N. Fyodorov IRTC «Eye Microsurgery», Ministry of Health of the Russian Federation, 10 Kolkhidskaya St., Novosibirsk, Russian Federation, 630096

List of references:

Paniagua D, Jiménez L, Romero C, Vergara I, Calderón A, Benard M, Bernas MJ, Rilo H, Roodt A, Suze D, Witte MH, Boyer L, Alagón A. Lymphatic route of transport and pharmacokinetics of micrurus fulvius (coral snake) venom in sheep. Lymphology. 2012;45(4):144-153.
Kim M, Johnston MG, Gupta N, Moore S, Yücel YH. A model to measure lymphatic drainage from the eye. Exp Eye Res. 2011;93(5):586-591. https://doi.org/10.1016/j.exer.2011.07.006.27
Goel M, Picciani RG, Lee RK, Bhattacharya SK. Aqueous humor dynamics: a review. Open Ophthalmol J. 2010;4:52-59. https://doi.org/10.2174/1874364101004010052
Johnson M, McLaren JW, Overby DR. Unconventional aqueous humor outflow: A review. Exp Eye Res. 2016;0014-4835(16):30016-1. https://doi.org/10.1016/j.exer.2016.01.017
Nakao S, Hafezi-Moghadam A, Ishibashi T. Lymphatics and Lymphangiogenesis in the Eye. J Ophthalmol. 2012. Avaible at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3317234/
Stolyarov GM, Lebedev OI, Zolotaryov AV, Karlova EV. Uveoscleral outflow of aqueous humor: theoretical aspects and research opportunities. Natsional’nyi zhurnal glaukoma. 2012;4:70-76. (In Russ.)
Lebedev OI, Stolyarov GM. Anatomic peculiarities of uveoscleral outflow (Literary review). RMZh. Klinicheskaya oftal’mologiya. 2011;1:7-9. (In Russ.)
Kalizhnikova EA, Lebedev OI, Stepanova EA, Trofimova EI. Changes in the topography of the anterior segment of the eye and uveoscleral outflow indicators in patients with primary glaucoma during cataract phacoemulsification. Natsional’nyi zhurnal glaukoma. 2015;14(4): 21-28. (In Russ.)
Yucel Y, Gupta N. Lymphatic drainage from the eye: A new target for therapy. Prog Brain Res. 2015;220:185-98. https://doi.org/10.1016/bs.pbr.2015.07.028
Borodin YuI. Lymphatic region and Regional limphodetoxication. Khirurgiya. Morfologiya. Limfologiya. 2004;1(2):5-6. (In Russ.)
Shmyreva VF. Lymphatic circulation in anterior segment with primary glaucoma. Vestnik oftal’mologii. 1986;4:8-12. (In Russ.)
Shmyreva VF, Petrov SY. The lymphatic vessels of the anterior segment with suspected glaucoma. Natsional’nyi zhurnal glaukoma. 2011;3:7-10. (In Russ.)
Petrov SYu. Lymphatic system of the eye. Glaucoma. 2014;3:58-62. (In Russ.)
Heindl LM, Kaser-Eichberger A, Schlereth SL, Bock F, Regenfuss B, Reitsamer HA, McMenamin P, Lutty GA, Maruyama K, Chen L, Dana R, Kerjaschki D, Alitalo K, De Stefano ME, Junghans BM, Schroedl F, Cursiefen C. Sufficient Evidence for Lymphatics in the Developing and Adult Human Choroid? Invest Ophthalmol Vis Sci. 2015;56(11):6709-6710. https://doi.org/10.1167/iovs.15-17686
Cursiefen C, Rummelt C, Jünemann A, Vorwerk C, Neuhuber W, Kruse FE, Schroedl F. Absence of Blood and Lymphatic Vessels in the Developing Human Cornea. Cornea. 2006;25(6):722-726. https://doi.org/10.1097/01.ico.0000214230.21238.3d
Cursiefen C, Schlötzer-Schrehardt U, Küchle M, Sorokin L, Breiteneder-Geleff S, Alitalo K, Jackson D. Lymphatic vessels in vascularized human corneas: immunohistochemical investigation using LYVE-1 and Pdpn. Invest Ophthalmol Vis Sci. 2002;43(7):2127-2135.
Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Radziejewski C, D’Amore PA, Dana MR, Wiegand SJ, Streilein JW. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest. 2004;113(7):1040-1050. https://doi.org/10.1172/jci20465
Peebo B, Fagerholm P, Traneus-Röckert C, Lagali N. Cellular-Level Characterization of Lymph Vessels in Live, Unlabeled Corneas by In Vivo Confocal Microscopy. Invest Ophthalmol Vis Sci. 2010;51(2):830-835. https://doi.org/10.1167/iovs.09-4407
Killer H, Jaggi G, Miller N, Flammer J, Meyer P. Does Immunohistochemistry Allow Easy Detection of Lymphatics in the Optic Nerve Sheath? J Histochem Cytochem. 2008;56(12):1087-1092. https://doi.org/10.1369/jhc.2008.950840
Herwig MC, Münstermann K, Klarmann-Schulz U, Schlereth SL, Heindl LM, Loeffler KU, Müller AM. Expression of the lymphatic marker Pdpn (D2-40) in human fetal eyes. Exp Eye Res. 2014;127:243-251. https://doi.org/10.1016/j.exer.2014.07.026
Yücel YH, Johnston MG, Ly T, Patel M, Drake B, Gümüş E, Fraenkl SA, Moore S, Tobbia D, Armstrong D, Horvath E, Gupta N. Identification of lymphatics in the ciliary body of the human eye: A novel «uveolymphatic» outflow pathway. Exp Eye Res. 2009;89(5):810-819. https://doi.org/10.1016/j.exer.2009.08.010
Birke K, Lütjen-Drecoll E, Kerjaschki D, Birke M. Expression of Pdpn and Other Lymphatic Markers in the Human Anterior Eye Segment. Invest Ophthalmol Vis Sci. 2010;51(1):344. https://doi.org/10.1167/iovs.08-3307
Borodin YuI, Bgatova NP, Chernykh VV, Trunov AN, Pozhidayeva AA, Konenkov VI. The structure of lymphatic capillaries of the ciliary body of the human eye. Morphologyа. 2015;148(6):43-47. (In Russ.)
Alm A, Nilsson S. Uveoscleral outflow: A review. Exp Eye Res. 2009; 88(4):760-768. https://doi.org/10.1016/j.exer.2008.12.012
Krebs W, Krebs IP. Ultrastructural Evidence for Lymphatic Capillaries in the Primate Choroid. Arch Ophthalmol. 1988;106(11):1615-1616.
Sugita A, Inokuchi T. Lymphatic sinus-like structures in choroid. Jpn J Ophthalmol. 1992;36(4):436-442.
De Stefano M, Mugnaini E. Fine structure of the choroidal coat of the avian eye. Vascularization, supporting tissue and innervation. Anat Embryol (Berl). 1997;195(5):393-418.
Xu H, Chen M, Reid D, Forrester J. LYVE-1 — Positive Macrophages Are Present in Normal Murine Eyes. Invest Ophthalmol Vis Sci. 2007;48(5):2162. https://doi.org/10.1167/iovs.06-0783
Schroedl F, Brehmer A, Neuhuber W, Kruse F, May C, Cursiefen C. The Normal Human Choroid Is Endowed with a Significant Number of Lymphatic Vessel Endothelial Hyaluronate Receptor 1 (LYVE-1) — Positive Macrophages. Invest Ophthalmol Vis Sci. 2008;49(12):5222. https://doi.org/10.1167/iovs.08-1721
Koina ME, Baxter L, Adamson SJ, Arfuso F, Hu P, Madigan MC, Chan-Ling T. Evidence for Lymphatics in the Developing and Adult Human Choroid. Invest Ophthalmol Vis Sci. 2015;56(2):1310-1327. https://doi.org/10.1167/iovs.14-15705
Chernykh VV, Druzhinin IB, Eremina AV, Khodjayev NS, Konenkov VI, Borodin YuI, Bgatova NP, Pozhidaeva AA, Trunov AN. The role of the lymphatic system in the uveoscleral outflow of aqueous humor. Oftalmohirurgiya. 2015;2:74-79. (In Russ.)
Chernykh VV, Borodin YuI, Bgatova NP, Nogovitsina SR, Toporkov IA, Eremin AV, AN Trunov, Konenkov VI The lymphatic structures in the ciliary body and choroid of human eyes. Sovremennye tekhnologii v oftal’mologii. 2016;3:268-270. (In Russ.)
Ramos RF, Hoying JB, Witte MH, Daniel Stamer W. Schlemm’s canal endothelia, lymphatic, or blood vasculature? J Glaucoma. 2007;16(4):391-405. https://doi.org/10.1097/IJG.0b013e3180654ac6
Karpinich N, Caron K. Schlemm’s canal: more than meets the eye, lymphatics in disguise. J Clin Invest. 2014;124(9):3701-3703. https://doi.org/10.1172/JCI77507
Aspelund A, Tammela T, Antila S, Nurmi H, Leppänen VM, Zarkada G, Stanczuk L, Francois M, Mäkinen T, Saharinen P, Immonen I, Alitalo K. The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel. J Clin Invest. 2014;124(9):3975-3986. https://doi.org/10.1172/JCI75395
Truong T, Li H, Hong Y, Chen L. Novel Characterization and Live Imaging of Schlemm’s Canal Expressing Prox-1. PLoS ONE. 2014;9(5):98245. https://doi.org/10.1371/journal.pone.0098245
Schlereth SL, Neuser B, Caramoy A, Grajewski RS, Koch KR, Schrödl F, Cursiefen C, Heindl LM. Enrichment of Lymphatic Vessel Endothelial Hyaluronan Receptor 1 (LYVE1)-Positive Macrophages Around Blood Vessels in the Normal Human Sclera. Invest Ophthalmol Vis Sci. 2014;55(2):865. https://doi.org/10.1167/iovs.13-13453
Schlereth SL, Neuser B, Herwig MC, Müller AM, Koch KR, Reitsamer HA, Schrödl F, Cursiefen C, Heindl LM. Absence of lymphatic vessels in the developing human sclera. Exp Eye Res. 2014;125:203-209. https://doi.org/10.1016/j.exer.2014.06.010
Schroedl F, Kaser-Eichberger A, Schlereth SL, Bock F, Regenfuss B, Reitsamer HA, Lutty GA, Maruyama K, Chen L, Lütjen-Drecoll E, Dana R, Kerjaschki D, Alitalo K, De Stefano ME, Junghans BM, Heindl LM, Cursiefen C. Consensus Statement on the Immunohistochemical Detection of Ocular Lymphatic Vessels. Invest Ophthalmol Vis Sci. 2014;55(10):6440-6442. https://doi.org/10.1167/iovs.14-15638
Pesin YaM, Borodin YuI. Vodnyi gomeostaz i limfotropnaya terapiya. Eksperiment i klinika. Bishkek: KRSU; 2015. (In Russ.)
Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med. 2012;4(147):147ra111. https://doi.org/10.1126/scitranslmed.3003748
Chernykh VV, Borodin YuI, Bgatova NP, Trunov AN, Khodzhaev NS, Nogovitsyna SR, Eremina AV, Konenkov VI Structural elements of the lymphatic drainage channels of the intraocular fluid in the human choroid of the eye in normal and with glaucoma. Oftalmohirurgiya. 2016;3:11-16. (In Russ.)

Close metadata