Cerebrospinal fluid absorption revisited: Do extracranial lymphatics play a role?

Neuroscientist

Volumn 6, Issue 2, 2000, Pages 77-87

  Johnston, M G ^a,b   Boulton, M ^a,b   Flessner, M ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Brain; Cervical lymphatics; Lymph nodes; Sheep; Spinal cord

Indexed keywords

ARTICLE; CEREBROSPINAL FLUID ANALYSIS; CEREBROSPINAL FLUID FLOW; HUMAN; HUMAN CELL; LYMPHATIC SYSTEM; MATHEMATICAL ANALYSIS; NEUROPHYSIOLOGY; TISSUE DISTRIBUTION; VOLUMETRY;

EID: 0033996783     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/107385840000600206     Document Type: Article

References (96)

1. Heisey SR, Held D, Pappenheimer JR. Bulk flow and diffusion in the cerebrospinal fluid system of the goat. Am J Physiol 1962;203:775-81.
2. Rubin RC, Ommaya AK, Henderson ES, Bering EA, Rall DP. Cerebrospinal fluid perfusion for central nervous system neoplasms. Neurology 1966;16:680-92.
3. Rubin RC, Henderson ES, Ommaya AK, Walker MD, Rall DP. The production of cerebrospinal fluid in man and its modification by acetazolamide. J Neurosurg 1966;25:430-6.
4. Cutler RWP, Page L, Galicich J, Watters GV. Formation and absorption of cerebrospinal fluid in man. Brain 1968;91:707-20.
5. Lorenzo AV, Page LK, Watters GV. Relationship between cerebrospinal fluid formation, absorption and pressure in human hydrocephalus. Brain 1970;93:679-92.
6. Key G, Retzius A. Anatomie des Nervensystems und des Bindegewebes. Stockhlom: Samson and Wallin; 1875.
7. Weed LH. The pathways of escape from the subarachnoid spaces with particular reference to the arachnoid villi. J Med Res 1914;31:51-9.
8. Weed LH. Forces concerned in the absorption of the cerebrospinal fluid. Am J Physiol 1935;114:40-5.
9. Clark WL. On the Pacchionian bodies. J Anat 1920;55:40-8.
10. Pollay M, Welch K. The function and structure of canine arachnoid villi. J Surg Res 1962;2:307-11.
11. Davson H, Segal MB. Physiology of the CSF and blood-brain barriers. Boca Raton (FL): CRC Press; 1996.
12. Del Bigio MR. Neuropathological changes caused by hydrocephalus. Acta Neuropathol (Berl) 1993;85:573-85.
13. Milhorat TH, Clark RG, Hammock MK. Experimental hydrocephalus. 2. Gross pathological findings in acute and subacute obstructive hydrocephalus in the dog and monkey. J Neurosurg 1970;32:390-9.
14. Clark RG, Milhorat TH. Experimental hydrocephalus. 3. Light microscopic findings in acute and subacute obstructive hydrocephalus in the monkey. J Neurosurg 1970;32:400-13.
15. Milhorat TH. Failure of choroid plexectomy as treatment for hydrocephalus. Surg Gynecol Obstet 1974;139:505-8.
16. Milhorat TH. Neurosurgery. In: Wilkins RH, Rengachary SS, editors. New York: McGraw Hill; 1985. p. 2135-9.
17. Milhorat TH, Hammock MK, Chandra RS. The subarachnoid space in congenital obstructive hydrocephalus. Part 2. Microscopic findings. J Neurosurg 1971;35:7-15.
18. Milhorat TH, Hammock MK, Di Chiro G. The subarachnoid space in congenital obstructive hydrocephalus. Part 1. Cisternographic findings. J Neurosurg 1971;35:1-6.
19. Raimondi AJ. Special comments on hydrocephalus. In: Ishii S, editor. Hydrocephalus. Amsterdam: Excerpta Medica; 1986. p. 167-70.
20. Gomez DG, DiBenedetto AT, Pavese AM, Firpo A, Hershan DB, Potts DG. Development of arachnoid villi and granulations in man. Acta Anat (Basel) 1982;111:247-58.
21. Gomez DG, Ehrmann JE, Potts DG, Pavese AM, Gilanian A. The arachnoid granulation of the newborn human: An ultrastructural study. Int J Dev Neurosci 1983;1:139-47.
22. Osaka K, Handa H, Matsumoto S, Yasuda M. Development of the cerebrospinal fluid pathway in the normal and abnormal human embryos. Child Brain 1980;6:26-38.
23. Fox RJ, Walji AH, Mielke B, Petruk KC, Aronyk KE. Anatomic details of intradural channels in the parasagittal dura: A possible pathway for flow of cerebrospinal fluid. Neurosurg 1996;39:84-91.
24. Nawar NNY. Observations on the pia-arachnoid of the anterior median fissure and the posterior median sulcus of the fetal spinal cord of the albino mouse. Acta Anat (Basel) 1980;108:30-3.
25. Winkelman NW, Fay T. The pacchionian system. Histologic and pathologic changes with particular reference to the idiopathic and symptomatic convulsive states. Arch Neurol Psychiatry 1930;23:44-64.
26. Gutierrez Y, Friede RL, Kaliney WJ. Agenesis of arachnoid granulations and its relationship to communicating hydrocephalus. J Neurosurg 1975;43:553-8.
27. Guthrie TC, Dunbar HS, Karpel B. Ventricular size and chronic increased intracranial venous pressure in the dog. J Neurosurg 1970;33:407-14.
28. Hammock MK, Milhorat TH, Earle K, Di Chiro G. Vein of Galen ligation in the primate. Angiographic, gross, and light microscopic evaluation. J Neurosurg 1971;34:77-83.
29. Haar FL, Miller CA. Hydrocephalus resulting from superior vena cava thrombosis in an infant. J Neurosurg 1975;42:597-601.
30. Rosman NP, Shands KN. Hydrocephalus caused by increased intracranial venous pressure: A clinicopathological study. Ann Neurol 1978;3:445-50.
31. Shulman H, Ransohoff J. Sagittal sinus venous pressure in hydrocephalus. J Neurosurg 1965;23:169-73.
32. Norrell H, Wilson C, Howieson J, Megison L, Bertan V. Venous factors in infantile hydrocephalus. J Neurosurg 1969;31:561-9.
33. Janny P, Chazal J, Colnet G, Irtum B, Georget A-M. Benign intracranial hypertension and disorders of CSF absorption. Surg Neurol 1981;15:168-74.
34. Sahar A, Hochwald GM, Ransohoff J. Cerebrospinal fluid and cranial sinus pressures. Relationship in normal and hydrocephalic cats. Arch Neurol 1970;23:413-18.
35. Shulman K, Yarnell P, Ransohoff J. Dural sinus pressure in normal and hydrocephalic dogs. Arch Neurol 1964;10:575-80.
36. Jones HC, Gratton JA. The drainage of cerebrospinal fluid in hydrocephalic rats. Z Kinderchir 1989;44(suppl 1):14-15.
37. Jones HC, Gratton JA. The effect of cerebrospinal fluid pressure on dural venous pressure in young rats. J Neurosurg 1989;71:119-23.
38. Greitz D, Greitz T, Hindmarsh T. A new view on the CSF circulation with the potential for pharmacological treatment of childhood hydrocephalus. Acta Paediatr 1997;86:125-32.
39. McComb JG. Recent research into the nature of cerebrospinal fluid formation and absorption. J Neurosurg 1983;59:369-83.
40. Van Deurs B. Structural aspects of brain barriers with special reference to the permeability of the cerebral endothelium and choroidal epithelium. Int Rev Cytol 1980;65:117-91.
41. Milhorat TH, Mosher MB, Hammock MK, Murphy CF. Evidence for choroid-plexus absorption in hydrocephalus. N Engl J Med 1970;283:286-9.
42. Cserr HF. Physiology of the choroid plexus. Physiol Rev 1971;51:273-311.
43. Lorenzo AV. Factors governing the composition of the cerebrospinal fluid. Exp Eye Res 1977;25(suppl):205-28.
44. Agre P, Brown D, Nielsen S. Aquaporin water channels: Unanswered questions and unresolved controversies. Curr Opin Cell Biol 1995;7:472-83.
45. Bradbury MWB, Cserr HF. Drainage of cerebral interstitial fluid and of cerebrospinal fluid into lymphatics. In: Johnston MG, editor. Experimental biology of the lymphatic circulation. Amsterdam: Elsevier Science Publishers B.V.; 1985. p. 355-94.
46. Brierley JB, Field EJ. The connexions of the spinal subarachnoid space with the lymphatic system. J Anat 1948;82:153-66.
47. Kida S, Pantazis A, Weller RO. CSF drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance. Neuropathol Appl Neurobiol 1993;19:480-8.
48. Courtice FC, Simmonds WJ. The removal of protein from the subarachnoid space. Aust J Exp Biol Med Sci 1951;29:255-63.
49. Bradbury MWB, Westrop RJ. Factors influencing exit of substances from cerebrospinal fluid into deep cervical lymph of the rabbit. J Physiol 1983;339:519-34.
50. Boulton M, Flessner M, Armstrong D, Hay JB, Johnston M. Lymphatic drainage of the CNS: Effects of lymphatic diversion/ligation on CSF protein transport to plasma. Am J Physiol 1997;272:R1613-19.
51. Cserr HF, Cooper DN, Milhorat TH. Flow of cerebral interstitial fluid as indicated by the removal of extracellular markers from rat caudate nucleus. Exp Eye Res 1977;25(suppl):461-73.
52. Cserr HF, Depasquale M, Patlak CS, Pullen RGL. Convection of cerebral interstitial fluid and its role in brain volume regulation. Ann N Y Acad Sci 1986;481:123-34.
53. Cserr HF. Role of secretion and bulk flow of brain interstitial fluid in brain volume regulation. Ann N Y Acad Sci 1988;529:9-20.
54. Bradbury MWB, Cserr HF, Westrop RJ. Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Physiol 1981;240:F329-36.
55. Yamada S, DePasquale M, Patlak CS, Cserr HF. Albumin outflow into deep cervical lymph from different regions of rabbit brain. Am J Physiol 1991;261:H1197-204.
56. Cserr HF, Knopf PM. Cervical lymphatics, the blood-brain barrier and the immunoreactvity of the brain: A new view. Immunol Today 1992;13:507-12.
57. Knopf PM, Cserr HF, Nolan SC, Wu TY, Harling-Berg CJ. Physiology and immunology of lymphatic drainage of interstitial and cerebrospinal fluid from the brain. Neuropathol Appl Neurobiol 1995;21:175-80.
58. Quirico Santos T, Valdimarsson H. T-dependent antigens are more immunogenic in the subarachnoid space than in other sites. J Neuroimmunol 1982;2:215-22.
59. Gordon LB, Knopf PM, Cserr HF. Ovalbumin is more immunogenic when introduced into brain or cerebrospinal fluid than into extracerebral sites. J Neuroimmunol 1992;40:81-8.
60. Boulton M, Young A, Hay JB, Flessner M, Armstrong D, Schwartz M, Johnston MG. Drainage of CSF through lymphatic pathways and arachnoid villi in sheep: Measurement of 125I-albumin clearance. Neuropathol Appl Neurobiol 1996;22:325-33.
61. Boulton M, Armstrong D, Mohamed R, Flessner M, Hay J, Johnston MG. Relative contribution of arachnoid villi and extracranial lymphatics to the clearance of a CSF tracer in the rat. Am J Physiol 1999;276:R818-23.
62. Boulton M, Flessner M, Armstrong D, Hay J, Johnston M. Determination of volumetric cerebrospinal fluid absorption into extracranial lymphatics in sheep. Am J Physiol 1998;274:R88-96.
63. Boulton M, Armstrong D, Flessner MF, Hay JB, Johnston MG. Raised intracranial pressure increases CSF drainage through arachnoid villi and extracranial lymphatics. Am J Physiol 1998;275:R889-96.
64. Foldi M, Csillik B, Zoltan OT. Lymphatic drainage of the brain. Experientia 1968;24:1283-7.
65. Csanda E, Obal F, Obal F Jr. Central nervous system and lymphatic system. In: Foldi M, Casley-Smith, JR, Schattauer Verlag FK, editors. Lymphangiology. New York: Stuttgart; 1983. p. 475-508.
66. Piller NB, Clodius L. Experimental lymphoedema: Its applicability and contribution to our clinical understanding. In: Johnston MG, editor. Experimental biology of the lymphatic circulation. Amsterdam: Elsevier Science Publishers B.V.; 1985. p. 189-230.
67. Weller RO, Kida S, Zhang ET. Pathways of fluid drainage from the brain - morphological aspects and immunological significance in rat and man. Brain Pathol 1992;2:277-84.
68. Rudert M, Tillmann B. Lymph and blood supply of the human intervertebral disc - cadaver study of correlations to discitis. Acta Orthop Scand 1993;64:37-40.
69. Löwhagen P, Johansson BB, Nordborg C. The nasal route of cerebrospinal fluid drainage in man. A light-microscopic study. Neuropathol Appl Neurobiol 1994;20:543-50.
70. Caversaccio M, Peschel O, Arnold W. The drainage of cerebrospinal fluid into the lymphatic system of the neck in humans. J Oto-Rhino-Laryngol 1996;58:164-6.
71. Russell DS, Rubinsten LJ. Pathology of tumours of the nervous system. 5th ed. London: Edward Arnold; 1989. p. 369-83.
72. Adair TH, Guyton AC. Lymph formation and its modification in the lymphatic system. In: Johnston MG, editor. Experimental biology of the lymphatic circulation. Amsterdam: Elsevier Science Publishers B.V.; 1985. p. 13-44.
73. Hogan RD, Unthank JL. Mechanical control of initial lymphatic contractile behavior in bat's wing. Am J Physiol 1986;251:H357-63.
74. Hogan RD, Unthank JL. The initial lymphatics as sensors of interstitial fluid volume. Microvasc Res 1986;31:317-24.
75. Bering EA, Salibi B. Production of hydrocephalus by increased cephalic-venous pressure. Arch Neurol Psychiatr 1959;81:693-8.
76. Benoit JN, Zawieja DC, Goodman AH, Granger HJ. Characterization of intact mesenteric lymphatic pump and its responsiveness to acute edemagenic stress. Am J Physiol 1989;257:H2059-69.
77. Li B, Silver I, Szalai JP, Johnston MG. Pressure-volume relationships in sheep mesenteric lymphatic vessels in situ: Response to hypovolemia. Microvasc Res 1998;56:127-38.
78. Eisenhoffer J, Lee S, Johnston MG. Pressure-flow relationships in isolated sheep prenodal lymphatic vessels. Am J Physiol 1994;267:H938-43.
79. Eisenhoffer J, Elias RM, Johnston MG. Effect of outflow pressure on lymphatic pumping in vitro. Am J Physiol 1993;265:R97-102.
80. Milhorat TH. Acute hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurg 1987;20:15-20.
81. Foltz EL, Ward AA Jr. Communicating hydrocephalus from subarachnoid bleeding. J Neurosurg 1956;13:546-66.
82. Kibler RF, Couch RSC, Crompton MR. Hydrocephalus in the adult following spontaneous subarachnoid hemorrhage. Brain 1961;84:45-61.
83. Ellington E, Margolis G. Block of arachnoid villus by subarachnoid hemorrhage. J Neurosurg 1969;30:651-7.
84. Fishman RA. Cerebrospinal fluid in diseases of the nervous system. Philadelphia (PA): WB Saunders Company; 1992.
85. Wandolo G, Elias RM, Johnston MG. Heme-containing proteins suppress lymphatic pumping. J Vasc Res 1992;631:248-55.
86. Elias R, Eisenhoffer J, Wandolo G, Ranadive NS, Johnston MG. Lymphatic pumping in response to changes in transmural pressure is modulated by erythrolysate/hemoglobin. Circ Res 1990;67:1097-106.
87. Elias RM, Eisenhoffer J, Johnston MG. Role of endothelial cells in regulating hemoglobin-induced changes in lymphatic pumping. Am J Physiol 1992;263:H1880-7.
88. Brace RA. Effects of outflow pressure on fetal lymph flow. Am J Obstet Gynecol 1989;160:494-7.
89. Gest AL, Bair DK, Vander Straten MC. The effect of outflow pressure upon thoracic duct lymph flow rate in fetal sheep. Pediatr Res 1992;32:585-8.
90. Johnson SA, Vander Straten MC, Parellada JA, Schnakenberg W, Gest AL. Thoracic duct function in fetal, newborn, and adult sheep. Lymphology 1996;29:50-6.
91. Smeaton TC, Cole GJ, Simpson-Morgan MW, Morris B. Techniques for the long-term collection of lymph from the unanaesthetized foetal lamb in utero. Aust J Exp Biol Med Sci 1969;47:565-72.
92. Wearden ME, Montgomery CA, Geske RS, Gest AL. Developmental histology of ovine thoracic duct. J Invest Med 1995;43(suppl 1):44A.
93. Marmarou A, Shulman K, Rosende RM. A nonlinear analysis of the cerebrospinal fluid system and intracranial pressure dynamics. J Neurosurg 1978;48:332-44.
94. Catala M. Carbonic anhydrase activity during development of the choroid plexus in the human fetus. Child Nerv Syst 1997;13:364-8.
95. Clark AH. On the fate of the jugular lymph sacs and the development of the lymph channels in the neck of the pig. Am J Anat 1912;14:47-62.
96. Jones HC. Drainage of cerebrospinal fluid during development and in congenital hydrocephalus. In: Segal MB, editor. Barriers and fluids of the eye and brain. Cambridge (UK): Macmillan Press; 1992. p. 116-27.