Vascular potential and thrombosis

TEW4BOSIS RCSURCH, Supplemat V; 73-82, 1983 0069-38wb3 $3.00 + .OO Printed in the WA. Copyright (c) 1983 Pcrguon Prcrt Ltd. All right8

VASCULAR

POTENTIAL

J.F. Remorheology

Department, Brabois,

SUMAHY

Ceutre

rercrved.

AND THROMBOSIS

Stoltz RSgional

54500 Vandoeuvre-l&s-Nancy,

de

Transfusion France

Sanguine

to the negetive ch8rge of The elrctrochemic81 phenom8u8 rcleted blood cells h8ve prwided ??mem8 of defining the iqmrtume of there p8rmehrr in vmculu thrabori8. of trmm patellIn puellrl with th888 work, na mtr tie1 heve roveeled that th8 vereel well 8180 carrier wtiv8 c&rger urd thur teker put in the ropulrim of blood cell8 aad pmveds

tbm

fra

Prirq

ad&riva

on tbo intiu.

Theme charger cm

fro verioor origin8 (ion or protein edrorpticm, 8ctive trmrfu through the vuculu veil, ioni8ed.poupr...). V88culu potential cm be 8pproaclwd by meen of vuiour technique8 trenmmae patentiel (eloctro-o8mo8i8), circul8tion potenti (in vitro 8ad in vim). On the krir of publirhed rerultr md hi8 own perlone rerearch, the different v8luer that beva beea obminod. th8 ruthor cmue8 Coruequently, it he8 been obremed tht the trenaembrem cherge mUTQt8 th8t Ue 8Cw88ibk Urirr( ?? hCtr -8i8 t8Ckliqu88 8nd St-1 pot8nti81 do reflact 8a8 di8CORdmee8 eccording t0 thewthOd8 wed. Ih irpor+PPW Of tbW8 p=8m@tOr8 8rd th put they’pl8y in thraborir phatartm i8 dircurtid.

IHTRCDUCTION Since tlm umk carried out by Abrmon (1) on the nrgetive charge of blood cell8, there h8ve been indicetiow tht tb ?? lectrochmiul pUaetU8 of tha blood Cell8 end varculu wall8 8hould be t&en into account in 811 ve8culu thrmbmir phawa8m (2.3). Ccmequently, N-t of struring potarti81 Of th8 blood VU8@18 (a)'bu revuled ebrt tb HIW1U ~811 cUri -getbe chuuer end thur taker pert in the r8pulrion of blood cell8, preventing them frr adhesion to the intiu (5). l&y Word8 : ~mctFokin8tic pheaamir - Strw fibrin lining - Thrombosis 73

potenti

- Endoendotheli81

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The origin of the surf ace charges is related to several mechanism8 : active transport through the membrane, msmbrane ions or protein8 adsorption, structure, ion and protein composition of blood, etc. These various factor8 play a suxe or less significant part in maintaining the negative charge of the vascular wall. Concurrently, the relationship between electric current and in vivo thraPr borir has been clearly revealed by Sawyer et al who showed that the appearance of thrombosis could be artificially induced or, on the contrary, delayed by subjecting the vessel wall to the action of a correctly oriented outside electric field (6,7,8). In addition, it has been observed that tissue lesion is apt to generate Moreover,

a current, blood

to an electro-kinetic in vivo determination umramant prwldes cular wall.

known as ‘lesion

current’.

in an electrically charged vessel giver rise phenomenon (9,lO) and Sawyer et al have carried out an of the current created (streaming potential) (11). This a quantitative approach to the charge density of the vasdisplacement

Apart from streaming potential, another manifestation of electrokinetic phemna in the vascular wall must be msntioned : that of the existence of tranandrane potential whose actual significance is not yet clearly known

(12).

It appears,

potentials

however,

would provide

that

the study of rtresming and transmsmbrane to thrombosis phenomena.

a new approach

In this wrk ve shall attempt to perceive the importance of these pheomesa in the origin of thrtiris phenm by defining the part played by plasma proteins and, in puticular, by fibrinogen on the msasured potentials. VASCULAE POTENTIAL MD namBOs1s 1. Iran&ran+

potential

As earl9 as 1824 Scudsmore (13) observed in vitro that blood precipitated on an electrode raised to a positive potential and at the ?? 0d of the 19th century Poor (14) and Skene (15) reported that a continuous current was apt to induce blaod coaylation and take put in the throlnbosis processes. The firrt modern studies on this subject were undertaken following the work carried out in 1951 by a team of Americaa surgeons who made intensive use of freeredried vareulu grafts os soldiers sent hcme from Korea (16,17). Contrary to all expectations, Pate and Sawyer obremed that these grafts behaved just as well, if not better, than the fresh grafts that had been used

up until

then.

In order to measure how rapidly transplanted tissues were reconstituted, they developed a technique consisting of measuring the difference in potential threugh the aortic wall in dogs (4). By capparing normal value8 with the of fresh ?? ud freezedried grafts they ware able to underline important points : - nom1 potential of the aortic wall of dogs in vivo was fouad to be betveen - 0.5 and + 0.5 mV, the sign indicating the charge of the intim as compard rith the ?? dventitia, - an electrode

implanted

in blood

cmpared with a second electrode the inversion of this potential

circulation

placed

is

often

on a negative potential , on the adventitia, and

takes

opposite

accompanied by

thrombosis,

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VASCXLABPOTEBJTIAL At?D TIBOngOSIS

- normel potential becoaing positive

can be altered or dertroyed by a lesion, as ccupuad with the adventitia,

75

with the intima

- fresh grafts are electrically active and after ipplant reveal very significant mlitude variations in potential. In contrast, after reconstitution graft contains no electric current at all, and rehydration, a freeze-dried whilot a 66~11 difference in potential with normal polarity appear6 around the 4th day after graft implant, - an analysis of the reeults related to thrombosis

ahowe that

the change6 in potential

It therefore remained to define whether vascular or the result of tbe potential reversal observed. 2. Vascular

potential

and prevention

thromboeio

are closely was the cause

of thrombosis

bwe results, it was interesting to find out whether On the basis of the ?? an electric current can be uaed for avoiding thr&eis by applying a difference in potential contrary to that of the ‘lesion currents’. The study wae carried out by Sawyer et al using various types of electrodes on dogs. A pair of vessels was chosen in each animal (femoral arteries or veins, external jugular vein6 and carotid arteries). An artificial lteion is madt in the two identical blood vessels by claaq~ing them with hemostatic forctpe for a givtn time, then fitting each vessel vith an eltctrode. One of the electrodes is connected to the negativt pole of generator ; tk collateral vteeel is fitted with an identical electrode, but as it is not subjected to the paisage of an tlectric current, it acts as the control. Kter the currtnt has passed through, tht veeetle art removed and are eubjtcted to histological examination ; a quantitative aeeeemnt is madt of tht dtgrtt of thrombosis. Analysis of the results revtale quitt significantly that thrombur formation is rtduced by applying negative potential (18).

3. Thrc&ogtnic

capacity

of an eltctric

current

Having obrtrved that a suitably polarized tlectric field can prtvent thra&us, Sawyer et al attempted a quantitative aeeesrment of the thrapboganic capacity of an electric currtnt. The study was carritd out on tht meeenttry of rats. Meeenttric vessels were observed with a microscope (19). An electric fitld can be applitd through the meeentery via a pair of electrodes placed at eithtr tnd. A second pair of eltctrodtr knoun te the ‘-muring electrodes, connected to a pottntiorPcttr, are used to tsetse the ?? quipotential field lines created by the applied electric field. The determination of the fitld lines crtated by a 20 microamp current, reveals that the drop in pottntial between the m6aeuring tltctrodee is approximately 20 millivolts, and thus tht veeeele are subjected to a differtnct in pottntial ranging fron 1 to 3 mv deptnding on thickness. Microscopic obeervation ehovs that blood cell precipitation, i.e. the start of thrabuo formation, affects almost all the vessels. This precipitation occurs first on the verse1 wall nearest the positive electrode. As long as the veeetl raina free frox lesion this early occlusion ie partially reversible by e*ly stopping the current. Eowever, if tht current is applitd for any considerable length of tim, irreversible occlusion of the vtertl occur6 , indicating that a currtnt

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POTKNTIALANDTlMlHBOSIS

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at low teasion, c6ncausa th6 occlusionof small ve66el6 of just a few PA, by blood cell deposit. In order to dofine the importance of these phewuna, Sawyer et al studied the precipitation potentialof blood calls.

CELL PREcIPITATIobl PvTmTxALm

CUmB

OF TEE vAscuLARuALLs

I. Precipitationpoteatialsof blood cells a) In vitro determinationof precipitationpotential : The in vitro precipitationof white blood cells, red blood cells, platelets and fibrinogenwas studiedunder various conceatratfoa, pE and ionic mediumconditions, in several specie6 including man and dog. The electrode is imersed in a transpareat chamber so that th cell deposit oa the surfaceof the electrodecan be observadthrough a aicroscopc. Humanred and white blood cell6 have the sam precipitationpotential (+ 0.33 2 0.02 v) colllpared vith a norm1 hydrogen electrode (3). These values

are determined at a pH of 7.4 in Krabs solution with ao anticoagulant. Recipitation is reversible and the potential is not dependeat on the type of electrode used, geaerally platinrn or gold ; but a change ia pH results in a change in potential. In this system, platelets precipitate irreversibly at + 0.42 2 0.2 v, with galling occuring imsdiataly (20). In contrast, platelet6 collected oa heparia no 1-r reveal just one precipitation potential, but precipitate over tha whole range of tension used. Eeparia appears to block fibrinogea-fibrin transfonsation, as the platelet6 do not precipitate. Ogoniak et al obserpedi that fibrinogen revulsd b&precipitated over a whole range of poteatial(21).

no critical

potential,

It caa thereforebe obssrred from these results that blood cells undergo a change in the membranerha in contact with aa electrode whose potential goes above a critical value. This phemmencmuould eppear to play sally put im thrumbo6i6 phemmena by reducing the density of the negative charge6 of tli8 vessel mll. b) In vivo dctexminatioa of precipitatiop

potential

:

In viva precipitation tests have been curied out oa dogs using carotid aad fwral arteriss (2). A platinum uire inserted into the vessel via a collateralartery, acts as the precipitation electrode, whilst a calm1 electroda measures t6s poteatial attained by the platinum wire. In this experimeat the arteries are usually the seat of thrombosis when the platinum wire reaches a potential above 200 - 300 mB. Thrombosis appurr to begin with platelet deposit. Substaaces tliat inhibit thrombosis also inhibitelectriccurrent-

induced thrombosis. 2) Charge of the vascular wall a) Electro-os~sis

:

Electro-owsis, which is an ?? lectrokiaoticphaumenon that occurs at a sol&+liquid i‘nterfaca, is defined as the movemeat of liquid through the pores of a membraneunder the influence of an electric field. An approach to

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VASCULAli POTgNTIALAND TEWMBOSIS

77

electro-osmsis can therefore be made by creating an electric field through a msmbrane and measuring the amount of liquid that parses through the membrathe zeta potenne. The flov rate measured provides the data for calculating tial, and the flow direction of the liquid indicates the sign of the charge. veal

The tests that :

for

assessing

this

potential

in different

vascular

valls

re-

- zeta potential value is not dependent on the area of wall mposed, and the volume of liquid transported per unit of time is a linear function of the applied electric field. These results are in accordance with theoretical hypotheses. vall,

- the increase

in pB produces

an increase

in the negative

charge

of the

- the orientation of the intims or adventitia towards one or other of only very slightly the flow of liths electrodes applyirg tension, modifies quid. Under normal conditions therefore, the vessel wall is shown to have a is dependent on pE ; mrewer, it can be alnegative charge. Its negativity tered by a lesion as well as by the existence of atherosclerosis in its final stage (22). b) Streaming potential

:

A solid that is in contact with an electrolyte solution generally acquiby ?? dsovptios of part of ions or molecules in the sores a surf ace charge lution (23). This is puticularly the case of blood cells, which have been the subject of a large nmber of studies. This is also true for blood vessels, with the appearance of an ionized double layer at the wall-blood interface.. When the fluid is put in mtion, the displacsmnt of positive charge as oppossd to the negative vessel wall will give rise to a Streaming Potential (24). Ths first in vivo strsaming potential msasuramsnts were carried out on th aorta and lower vena cuva in rats, then in rahbits. The wasurmnt of the streaming potential was carried out in conjunction with blood flow measurent, venous or arterial pressure and electrocardiogram, thus providing a msans of studying the variations brought about by these parameters (25,26). Ths author himself used two methods for approaching this with an -dance rabbits, using either glus micro-electrodes 10 - 30 mgohm, or platinm electrodes implanted via collateral results revealed scatter of the values observed, which ranged with the glass electrode method and from 10 to 20 mV with the trades.. These values are in agr cement with those observed by using rats or rabbits.

potential in ranging from vessels. The fraa 10 to 50 mV platinum elecother authors

It should, however, be noted that although the values observed are within the sm range, they differ from one masuring method to the other and f r?q 00~ animal to the other. On the basis of these streaming potential values, the ssta potential can be calculated with ~luchovski’s equation, which is gemrally used and which connects seta potential with streaming potential.

VASCIJLU

c

7 K D

AP v‘ fied,

Suppl.

POTBNTIALAND TBBOHBOSIS

in mV = viscosity in poise (0.027 for blood) = rpecific conductivity (2 x log for rabbit’8 blood) - dielectric constant (120 at 25*C, 74 at 37.C) - difference in prerrure between the two mearuring electrodes - rtreaming potenti in mV.

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1983

- zeta potential

By introducing the value8 of the constant‘ , the equation giving, in the case of rabbit’8 blood at 37*C : 7

- 9.16

(in dyne8/cm2)

can be simpli-

IO6 ‘8 z

In order to obtain the zeta value from electro-osmo8i8 term V /AP mat be replaced by Q li, where : 9 is the flow me&de in ml/second and i ir the current applied, in -8.

experiment8 the rate through the

By applying Sololuchovski’r equation, the zeta potential of the aorta and vena cava of rabgitr cm be calculated a8 being ?? pproxi~tely 200 mV and the zat8 valuer calculated on the baris of electro-ormotic flow rate, range between -3 -10 mV, i.e. approxtitely 50 timer lower than the above rerultr. The values obtained frm circulation potential measurement do not see81 to agree with the zeta valuer calculated by tlectro-o=ris measurmnt on blood vtrrelr in dogs. In fact, this diragremnt is only apparent, as the first method measures the transve88el zete potential and is therefore connected with transport phenomena, whilst in the recond nuthod the potential ir conaected vith the ktim and ir consequently responsible for cellular adherion phenomsna. 3) Origins

of the surface

charges

of

the verrtlr

Since no uulyt2c rtuditr have been carried out, contrary to the case for blood cell8 (27), it is at present no easy mtter to define the origin and nature of the observed vascular electrokinetic phenonsna. Although it tight be ?? ssumsd that the exi’rtence of r’onized groups is partly responsible for.thc measured potential‘, the other part might be due to the prerence’of endoendothelial fibrin lining (EEPL), ass& by Copley (28,29,30,31). On the bar58 of this hypothesis, we have revealed in a recent study uring alternating streaming current (32). that the outface potential of ?? lectropo8ihemocoapatiblt mterials wa8 increared in abrolute tive or electronegative value, (with a change of sign for the electroporitive Puterialr),after conuspensions containing albdn or fibrinogen. tact with plasma or protein ?? Concurrently, the study on adsorption of these protein8 reveal8 that there rurfacer heve an affsnity 4 to 5 tin2 a gruter for fibrinogen than for albumin (e.g. 0.2 kge/us v8. 0.04 g/cm for the electropositive material PAC) and a decrease in platelet adht rion (33).

In conclusion, the results reported in this paper confim the existence of varcular potentr’818 (stresming potential or trm&rum potential) whora rignifr’cmce in thraborir phenane must not be disregarded, although the

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VAXULARPCl’RNTLALARD TMlOMBCSIS

79

origin of the charges has yet to be defined. However, the resulto obtained using bexmmpatiblc materials allov a diagramatic rcpromtatioa of the oricells, as do blood cells, gin of the charge to be put forward : endothelial might contain positive or negative ionized groups OD which the plasma proteins, and particularly fibrinogen, become attached (fig.). Trm AbOntitial

potomi*t

Tunk

FIG. Rypothetic representation of the influence of the EEFLon the electroki_ . (wdified from Copley Rypotherir) nrtic properties of the vessel wall. Tbir adsorbed layer could be at the origin of Eel. and might be a determining factor in the value of the observed potentialr, which according to Oka (34.35) would provide an explanation for the decreare in apparent blood vircoeity of fibrin coated tuber (‘Copley-Scott Blair phenolunon’). With regard to tranme&rane potential, it would also be of interert to couridex rtudying thi% parameter in connection with varcular permeability. the porrible dependence Indeed, &he ruultr given abwe would Beem to indicate of thir potenttal ou traurparietal exchange pMua. In thir case, it would be of particular importance to study the porsible action of plasm8 pmuins or certain mleculer that are released during the traneformation of fibrinogen to fibrin mumera. This work vas supported

by DIET (Biological

department)

RRPRRRMXS 1. m,

B.A. The electrophorerio of the blood platelets of the horre with reference to their origin and to thrunbus formation. J. Exp Med. 47 677-683, 1928.

2. BROWN,J.C., LAVELLE, S.H. and SAYPEB, P.N. Ralatiowhip and rpontaneous thromborir. l’hraab. Diath. Ramor., 21,

between electrical 325-331, 1969.

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VABCULARPOTBllTIALAHDTBK&&BOSIS

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3. SAWYER,P.N., RRATTAIN, W.R. and BODDY, P.J. Electrochemicalprecipitetion of human blood cell8 and itr porriblerelation to intravarcular throeboris.Proc. Nat. Acad. Sci, Sl, 428-432, 1964. 4. SAWYKR,P.N.and PATE, J.W. Electricalpotentialdifference8act088 the normal aorta and aortic graft8 of dogr. her. J. PhySiOl.175, 113-117, 1953. 5. I&CAN, A., STOLTZ,J.P., NICIAUSK,H. and STREIPP,F. IntroductionB l'gtudede8 ph&u&ner 6leCtrOCin6tique8. Application8P la aurpenrion sanguineet B 1'iZtude du ryst&8 varculaire.Agre880108ie,11, 317-325, 1970. 6; SAWYER,P.N. and DEUTCE, B. Use of electricalcurrent8 to delay intrava8cular thromborisin experimentalanimelr.Am. J. Phyriol.187, 473-478, 1956. 7. SAWYER, P.N., SUCKLING,E.E. and WRSOLOWSKI,S.A. Effect of 8znallelectric current8on intravarcularthromboririn the visuelitedrat merentery. Amer. J. Phy8iOl.198, 1006-1010,1960. 8. SAWYER,P.N. and VeSOLOWSKI,S.A. The electriccurrentof injured tirrue and varcularocclusion.Surgery,g, 34-42, 1961. 9. CIGNITTI,M. Streemingpotential8: theory and exwle8 ryrtem8.Experientia,18, 25-33, 1971.

in biological

10. SK&AN, G.V.P. Electrokineticmethod8 in the rtudy of biologicalrmfacer. In : Theoreticaland CIinicaltitheolo~ A.L. Copley and E.H. Bartert (Edr) Heidelberg,SpringerVerlag, 1969, pi 242-252. 11. SAWYKR,P.N. and BIMIBLFABB, E.E. Studiesof rtreamingpotential8in large -lien blood verrelr in vivo. In : Biophy8icalMecheaiu in VascularEomeo8tariraud krttevuculu TbromborirP.N. Sawyer (Ed.) New York, Meredith, 1965, pp 69-75. 12. EARSHM, D.H. and SAWYER, P.N. Electroomtic characterirticrof mamalian aorta and vena cava. In : BiophyricalHechulirmrin Varcularbm8ta8i8 and Intravo8cularTbrombo8i8,P.N. Sawyer (Ed.) New York, Meredith, 1975, PP In-68

13. SCUDAMORE,C. EIsay on the Blood. London, Longham,liurrt,Beer, Orme & Green, 1824. 14. POORE, G.V.A. Textbookof Electricityin Medicine and Surgery.London, Smith, Elder & Co, 1876. 15. SKBNE,A. Electra-Baewrtaririn OperativeSurgery.New York, Appleton a Co, 1899. 16. PATE, J.W. and SAWYER,P.N. Pre88e dried aortic graftr.A preliminary report of the experimentalevaluation.Am. J. Sure, 86, 3-9, 1953. 17. PATE, J.W., SAWER, P.N., DETRRLING,R.A., BLUNT, W., and PABSBLEY M.S. Early rerultr in the experimentalu8e of freeze-driedartarialgrafts. Sum. Forum, g, 147-153,1952.

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VASCULARPOTgNTXALAND TRRCHBOSIS

18. SAWYER,P.N., and PATE, J.U. in intravarcular throPPbori8. 19. SAWYER, :f;ld;g;; 9

81

Biolcctric phenollaua a8 rtiologic Surgery, 34, 491-497, 1953.

P.N., and DEUTCH,B. The experimental use of oriented delay and prevent intravarcular thrauboris.Surg.For~ .

20. SAUYEB, P.N., REARDON,J.H. and OGONIAK,J.G. Irreversible cal precipitation of mamalian platelets and intravascular Proc. Nat. Acad. SC., 2, 200~207, 1965.

electrical 2, 173-

electrochemithrombosis.

21. OGONIAK,J.C. and SAUY?lR, P.N. The electrochemical precipitation brinogen. Proc. Nat. Acad. Sci., 53, 572-575, 1965. 22. SAWYER,P.N., SETO, S. and SRINIVASAN, S. Electrokinetic of normal and atherosclerotic human aortae. Surrery,g,

factors

of fi-

characteristics S2irg28, lf67.

23. TEORELL, T. The role of electrical force8 at cell boundaries. In : Biophysical McchanirrPr in Varcular Holreostarir and Intravascular ThromGis P.N. Sawyer (Ed.) New York, Appleton Century and Appleton Century Crofts, 1965, pp 19-29. at the interface 24. JONES, G. and WOOD,L.A. The measurement of potentials between vitreous silica and 8olutions of potassium chloride by the streaming potential method. J. Chem. Phyr. 13, 106-112, 1945. 25.

SAWYER,P.N., -LFARB, E.H., LUSTRKN, I. and ZISKIND, B. Measurement of streaming potentials of mlian blood verrels, aorta and vena ceva, in vivo. Biophyr. J., 5, 641~651, 1966.

26. SRINIVASAN, S,, Determination of carotid artcrier centrations. J. 27.

BURROWES,C.B., LUCAS, T., RAURR, S.B. and SAWYER,P.N. in vitro rtreamiug potential8 through canine aortae and with variation of internal and external electrolyte conBiomed. Mat. Res. 1, 355-362, 1967.

STOLTZ, J.P. Ionized or ionizable group8 of blood cells. In : The rheology of blood, blood verrelr and ?? 88ociated ti88ue8, D.R. Grow and M.N.C. Euang (Eds.) - NATO Advanced Study Inrtituter Series (Rochville, U.S.A.) Sijthoff Noorddhoff, Applied Science8, Serie E, 41, 184-213, 1981.

28. COPLEP, A.L. On the endoendothelial fibrin layer, fibrin(ogen) polymerization, and thromboris. In : Blood Ve88cl8, Problem8 Arising at the Bardarr of Natural and Artificial Blood Ve88elr. S. Effert and J.D. HeyerErkelenz @de.) Berlin-Eeidelberg-New York, Springer Verlag, 1976, pp 21-27 29. COPLEY, A.L. and KXNG, R.G. Polymolecular layers of fibrinogen systems and the genesis of thrombosis. In : liemorhcology and Thrombosis. A.L. Copley and S. Okamoto (Eds) (Oxford New York), Pergamon Press, 1976, pp. 393-409 ; Thrombori6 Res. s, suppl. II, 393-409, 1976 significance of hemorheological aspects 30. COPLEY, A.L. Tathophyoiological of ?? ndoendothelial fibrin lining and of fibrinogen gel clotting. In : Remrheology and Di8ea8es. Proc. 1 European Symporium, Nancy, France 17-19 October 1979. J.F. STOLTZ and P. Drouin (Eds.) Paris, Doin Editeurs, 1980, pp. 293-325.

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31. COPLEY, A.L. Remorheological ?? zpecta of the endoendothelial fibrin lining fibrinogen gel clotting. Their importance in phyriology and paand of thological conditioar. Clinical Hemorheology, r, 9-72, 1981. 32. GROVES, J.N. and SUM, A.R. Alternating J. Coll. fnterf. Sci., 53, 83-89, 1975.

rtreaming

current

meazurementz.

et potentiel 33. USHIDA, T., FUNARUBO,8. and STOLTZ J.F. HemocompatibilitB zbta. Influence de l’albmiae et du fibrinogine 8ur l'tihb8iOn plaquetI.T.B.M. 5, (in preso), 1983. taire. Blair 34. OKA, S. Copley-Scott logp, 18, 347-354, 1981.

pbnomenon

and electric

35. OKA, S. Some rurface phenomena in clinical rheology, 2, 3-6, 1902.

double

hemorheologp.

layer.

Biorheo-

Clinical

Hemo-