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J. Electron Microsc, Vol. 32, No. 1, 33-44, 1983

Tridimensional Architecture of Elastic Tissue in the Rat Aorta andFemoral ArteryA Scanning Electron Microscope Study

Kojiro W A S A N O and Torao YAMAMOTODepartment of Anatomy, Faculty of Medicine, Kyushu University,3-1-1, Maidashi, Higashi-ku, Fukuoka, 812 Japan

(Received January 6, 1983; accepted M arch 10, 1983)Overall tridimensional architecture of the elastic tissue in the rat aorta (elastictype artery) and femoral artery (muscular type artery) has been studied byscanning electron microscopy after hot-formic acid extraction followed byfreeze-drying method. In the aorta the elastic tissue is composed to 6-7concentric plate-like laminae interconnected by radially oriented interlaminarelastic fibers, whereas in the femoral artery it is composed of two distinctinner and outer sheet-like laminae bridged by a dense continuous interlaminarnetwork of elastic fibers. The internal elastic lamina has numerous fenes-trations which considerably differ in size, shape and structure between thetwo types of arteries . Tunnel-like compartments free of elastic tissue extendhelically into the medial wall of both types of art eri es . These findings arediscussed in relation to conventional transmission electron microscopic in-formation and some new functional roles of arterial elastic tissue are pro-posed.

Key words= scanning electron microscopy (SEM): elastic tissue: aorta andfemoral artery: rat: formic acidI NTRODUCTI ON

Elastin is the major structural componentof the medial connective tissue at variouslevels of arteries. Measurements of theelasticity and tensile strength of whole arterialtissue1"41 and of pure elastic tissue isolatedfrom the arterial tissue 5" 8 ' have indicated thatthe elastic tissue is involved in the static anddynamic mechanical properties of arterialwalls. For a better understanding of itsmechanical behavior in response to externalstresses applied to arterial walls, it seemsessential to know the overall tridimensionalarchitecture of the elastic tissue near its in vivoform. Conv entional light and transmissionelectron microscopy (LM and TEM) are oflittle use for this purpose, since these methodspermit no estimation of the spatial relationshipsof such an intricate structure due to the thin-ness of the sections . Sca nning electron micros -copy (SEM), however, is eminently suited forvisualizing tridimensional images, since it

provides a much larger focal depth than LMand TEM.

To visualize arterial elastic tissue underSEM, it is necessary to remove selectively othertissue components in arterial walls, includingcollagen fibers, ground substances, smoothmuscle cells and other cell components.Several techniques have been developed forisolating pure elastin in past studies.9"14 'Among these techniques, hot-formic acidextraction method9 ' was used in this study,since the method has several advantages inthe following po ints. (1) It ha s been showntha t perfusion-fixation of arterial tissues at aphysiological pressure is necessary to preservethe structural organization of the elastic tissuenear its in vivo condition. 3 ' Only hot-formicacid can be used for the isolation of elastictissue from fixed tissue materials.15 ' (2) It isa single-step extraction method which candissolve all other tissue components in arterialwalls except the elastic tissue.7 '9 ' This can

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34 K. W ASA NO a nd T . YAMAMOT O

minimize mechanical damages on the delicatenetwork of the isolated elastic tissue whichmay be unavoidable in other multi-step ex-traction techniques. (3) The structural integ-rity of elastic tissue has been shown to bepreserved during long extraction periods upto 400 hr. 7 '9 ' This slow extra ction rate per-mits the delicate regulation of extraction dura-tion necessary for the degradation of only non-elastic tissue components.

Removal of water from the isolated elastictissue is the second critical step necessary forSEM examination, since the structural in-tegrity as well as the mechanical property ofelastin is known to largely depend on its watercontent.16 ' In the present study, freeze-drying method was used, instead of criticalpoint drying method, to avoid distortion andshrinkage artefacts due to the interactionbetween purified elastin molecule and organicsolvents during dehydration process.17 '

Using these techniques, the present studydemonstrates the overall architecture of theelastic tissue in two different types of arteriesof the rat.

MATERIALS AND METHODSAdult male WKA rats , four months of age

and weighing abo ut 250 g, were used. Allthe animals were sacrificed by intraperitonealinjection of p entob arbital (30 mg/kg) andperfused from the left ventricle with fixativesolution containing 4% paraformaldehyde in0.1 M pho sph ate buffer (pH 7.4) at a cons tantpressure (120 mm Hg ) for abo ut 20 min. Afterthe perfusion fixation, the segments of theabdominal aorta between the levels of therenal and ileolumbar arteries, and the femoralarteries between the branching points of thesuperficial circumflex iliac and superficialepigastric arteries were dissected out andimm ersed in the sam e fixative for 24 hr at4C. After careful removal of extraneousadventitial tissue with a fine forceps under abiocular microscope, the tissue specimens wereprocessed for subsequent transmission and

scanning electron microscopic preparations.Transmission electron microscopy. To ex-

amine the general structure of intact arterialwalls, some segments of the aorta and femoralartery were cut into small rings and fixed in3 % glutaraldehyde in 0.1 M pho sphate buffer(pH 7.4) for 2 hr.

To determine the least extraction period,the segments of the aorta and femoral arterywere cut transversely with razor blades intotwo hundred cylindrical rings of about 1 m min length and divided into ten groups respec-tively. Each gro up was separately incub atedin glass-stoppered vessels conta inin g 5 ml of8 8% formic acid at 45C for various periodsof time of 24, 36, 48, 60, 72, 84, 96, 120, 168and 216 hr. In proportio n to the incubationtime, the arterial rings become transparent andswollen. After the incu bati on, five rings werewashed in 0 . 1 M phosphate buffer (pH 7.4)and immersed in fixative solution containing3 % glutaraldehyde and 2% tannic acid in thesame buffer for 30 min. The othe r fifteenrings were processed for subsequent scanningelectron microscopic preparations.

After a brief rinse in 0.1 M phosphate buffer(pH 7.4), the tissue specimens were postfixedin 1 % osmium tetroxide in the same bufferfor 1 hr, dehydrated in graded ethano ls and em-bedded in Epoxy resin. Ultra thin sectionswere stained with 2% uranyl acetate in 50%ethanol and lead hydroxide with or withoutprior staining in 2% aqueous tannic acid solu-tion, filtrated through a Sartorius membranefilter of 5 nm por e (Zeiss, W est Ge rm any )before use, for 15 min and exam ined in aHitachi Hu-I2A transmission electron micro-scope.

Scanning electron microscopy. The isolatedelastic tissue were carefully washed in severalchanges of 0.002 N HC1 until they retu rne dto their original dimensions according to themethod of Kuhn,15 ) since washing in neutralbuffer results in a shrinkage of the tissue to aconsiderable extent. The tissue specimenswere rapidly frozen in liquid nitrogen andfreeze-dried in a JEE-5S vacuum evaporator


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Tridimensional A rchitecture of Arterial Elastic Tissue

Fig . 1. (A) A cross-sectional view of an intact ao rtic wall. Th e elastic tissue (stained black with tannicacid) is composed of 6-7 concentric elastic laminae and fragmental cords of interlaminarelastins. The internal and external elastic laminae are thinner and more discontinuous than theother m edial elastic laminae between them. L: vascular lumen, A : adventitia. (B) A trans-mission electron micrograph showing the structure of an aortic wall incubated in hot-formicacid for 96 hr. All the structural com ponen ts of the vascular wall except the elastic tissue (stainedblack with tannic acid) are completely removed. L: vascular lumen, A: adventitia. x2,1 00 ,Scale bar=5 /im.



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36 K . W A S A N O a n d T . Y A M A M O T O

under a vacuum of 10 5 Torr in the presence ofP 2O 6 as a water tra p. The dried specimens werecarefully affixed on aluminum stubs withdouble-sided sticky tape, coated with about100A thick gold-palladium alloy in an EikoIB-5 ion sputter coater and examined in aHi tachi S-430 scanning electron microscope.Stereo-pair photographs were taken at 7 til tangles.

RESULTSTransmission electron microscopy

In thin sections routinely stained with uranylacetate and lead hydroxide, the discernmentof the amorphous elastin from other extra-cellular tissue components is difficult, since itremains unstained with these two metal saltsas an electron-lucent homogeneous structure.Prior staining with tannic acid, however, con-siderably enhances its electron-density, makingit possible to survey the overall morphologyof the elastic tissue easily. Th us , the follow-ing findings were obtained from thin sectionsstained with tannic acid, uranyl acetate andlead.

General structure of intact arterial walls. Inthe aorta, the elastic tissue is composed of 6-7concentric laminae oriented in roughly paralleldirec tion (Fig. 1A). Each lam ina is 1-2.5 /*mthick and disposed 5-20 /


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Tridimensional Architecture of Arterial Elastic Tissue J fbund les pass. The medial wall between the except the outer few sm ooth muscle cell layerstwo elastic laminae is predo min antly occupied running in parallel direction to the longitudinalby closely packed sm oo th muscle cell layers axis of the artery (Fig . 6A ).with isolated fragmen tal elastic fibers (Fig . In both types of arter ies, the adve ntitial6A). Mo st of the sm ooth muscle cells are elastic tissues show similar organ ization, con-arra nge d obliquely to the plane of section sisting of sparsely dispo sed elastic fibers.

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Fig. 3. (A) A scanning electron micrograph showing the luminal surface of the aortic internal elasticlamina . The internal elastic lamina has num erous large fenestrations irregularly crossed by finebranching anastomosing elastic fibers. (B) A transmission electron microscopic image of theaortic internal elastic lamina (IEL). The internal elastic lamina has large fenestrations inter-rupted by only dot-like or fibrous elastins. Form ation of myoendothelial junctions through thefenestrations can hardly be seen. E : endothelial cells, S: medial smooth muscle cell, L: vascularlumen. (A) X 880, Scale bar = 10 //m, (B) x 4,200, Scale ba r = 2 /im.Fig. 4. A scann ing electron micro graph show ing the adventitial half of the aortic elastic tissue viewedfrom oblique adventitial direction. The medial elastic laminae have small round fenestrations(arrow s) with various sizes, aste risk: external elastic lamin a, x 760, Scale bar = 10 //m.Fig. 5. A scanning electron m icrograph showing the adventitial surface of the aortic elastic tissue. Theadventitial elastic tissue consists of a randomly tangled network of fine elastic fibers giving offbran ches tha t are directly joined with the surface of the subjacent external elastic lamina (asterisk),x 1,000, Scale bar = 10 pm .



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Tridimensional Architecture of Arterial Elastic Tissue IS

Fig. 6. (A) A cross-sectional view of the wall of an intact femoral artery . The elastic tissue (stained blackwith tannic acid) is poorly developed as compared with that in the aorta shown in Fig. 1A.Jn this type of artery, however, the internal elastic lamina is remarkably developed and appearsas an almost thick contin uou s sheet. The medial wall is predo minantly occupied by closelypacked smooth muscle cells layers interspersed with isolated fragments of interlaminar elastins.L : vascular lumen, A : adventitia. (B) A transmission electron micrograph showing the structureof the wall of a femoral artery treated in hot-formic acid for 72 hr. All the non-elastic tissuecomp onents are completely digested. L: vascular lumen, A: adven titia. x2 ,100 , Scale ba r= 5 fim.



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They are closely associated with long slenderprocesses of adventitial fibrocytes that arewidely separated by wavy thick adventitialcollagen fiber bundles (Figs. 1A and 6A).Structure of formic acid-treated arterialwalls. In both types of arteries , the a mo rpho usground substances and all the cell componentswere completely dissolved after initial 36hr of extraction in hot-form ic acid. Collagenfibers are the most resistant component againstformic acid and persist for a longer time thanthe other non-elastic tissue com pon ents. Thepersistence appears to vary with the thicknessof the arterial wall and the compactness ofits structu re. In the femoral arte ry all thecollagen fibers disappeared between 60 and 72hr (F ig. 6B), while in the a ort a 84 to 96 hr ofextraction was necessary for complete removalof the collagen fibers (Fig . 1B). N o detectablechange of the organization of the elastictissue occurred for further extraction perioduntil the end of 120hr, but more prolongedextraction resulted in the partial enlargement

of the spaces between adjacent elastic laminaeprobably due to the degradation of fine elasticfibers interconn ecting them . Th e elastictissue, however, fully retained its affinity fortannic acid and appeared homogeneous oralmost amorphous in texture after prolongedextraction time up to 216 hr.Scanning electron microscopy

The preliminary TEM study has revealedthat the least extraction time is 72 and 96 hrin the femoral artery and aorta respectively.Thus, the following SEM observations weremade on these materials.The removal of non-elastic tissue compo-nents with formic acid treatment unveiled withgreat clarity the structure of the arterial elastictissue. The mo rpho logy of the elastic tissueis considerably different between the aortaand femoral artery.

In the aorta, the elastic tissue is composedof 6-7 concentric laminae interconnected witheach other by interlaminar elastic fibers (Fig.

Fig. 7. Stereo scanning electron micrographs showing the tridimensionalarchitecture of the elastic tissue in the formic acid-treated femoralartery. The elastic tissue is composed of two distinct internaland external elastic laminae interconnected with each other bya dense continuous network of branching anastomosing elasticfibers. Note that tunnel-like compartments extend obliquelyinto the arterial wall from left to right direction . The externalelastic lamina splits into double layers, surrounding an elastin-poor compartment (asterisk) which extends into the arterial wallin parallel to its longitudinal axis. L: vascular lumen, A: ad-ventitia. x 1,050, Scale bar= 10 //m.Fig. 8. (A) A scanning electron micrograph showing the luminal surfaceof the internal elastic lamina of the femoral artery. The internalelastic lamina has numerous small round fenestrations traversedby a few crosscut elastic fibers. (B) A transmission electronmicroscopic image of the internal elastic lamina (IEL) of thefemoral artery . The internal elastic lamina has simple narrow gapsthrough which endothelial cells (E) frequently give rise to slenderprocesses to form myoendothelial junctions with the underlyingmedial smoo th muscle cells (S). L: vascular lumen. (A) x87O,Scale bar=10/


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Tridimensional Architecture of Arterial Elastic Tissue 412A). The laminae appear as solid sheet-likestructures, about 1-2.5 jum in thickness, thatare arranged in almost parallel, althoughsomewhat irregularly undulated, at intervalsof about 5-20 fim (Fig. 2A, B and C). TheIEL has numerous large oval fenestrations ofvarying diameter from 50 up to 200 /xm (Figs.2B and 3A). The fenestrations are irregularlycrossed by fine branching anastomosing elastic

fibers, being divided into small pores withvarious sizes and shapes (Fig. 3A). Thefenestrations are randomly distributed, withtheir long axes running in different directions,indicating that they have no special relation-ship to other non -elastic com pone nts, especiallyendothelial cells which closely covered thesurface of the IE L before the extraction. TheEEL does not form a continuous sheet, but



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consists of extensively fenestrated disk-likeplates and branching anastomosing network ofelastic fibers arising from their margins (Figs.2C, 4 and 5). The medial elastic laminae,although having round fenestrations of about5-10 fim in diameter, appear as almost thickcontinuous sheets (Figs. 2B, C and 4). Allthese elastic laminae are interconnected witheach other by radially oriented interlaminarfibrous or fenestrated septum-like elastins.They are often arranged in parallel rows justlike roadside trees, resulting in the formationof tunnel-like compartments free of elastictissue which extend into the aortic wall in thesame helical direction (Fig. 2A, B and C). Inthe outermost interlaminar space, however,only sparse fine elastic fibers bridge betweenthe adjacent laminae without making obviouscompartments as mentioned above (Fig. 2C).The adventitial elastic tissue is composed of acomplicated network of randomly tangledfine elastic fibers of about 1 fim in diameter.There fibers are evidently linked with the disk-like plates or fibrous elastins constituting theaortic EEL (Figs. 2C, 4 and 5).

In the femoral artery, the elastic tissue isbasically composed of two distinct 1EL andEEL that are interconnected with each otherby a complicated interlaminar elastic fibernetwork (Fig. 7). The IEL appears as aslightly undulated thick plate-like structure,about 2 fim in thickness, and has numeroussmall round fenestrations, varying in sizefrom 1 to 5 fim (Fig. 8A). The fenestrationsare uniformly distributed throughout the IELand are sometimes divided by a few crosscutelastic fibers into a few partitions. The EELshows a slightly undulated sheet-like structure,about 1 fim in thickness, having numerousfenestrations similar to those seen in the IEL(Figs. 7 and 9). In some places, the EELis split into double layers, surrounding anelastin-poor compartment which extends intothe arterial wall parallel to its longitudinalaxis (Fig. 7). Although the IEL and EEL aredisposed in an almost parallel fashion, about30-35 fim apart, their undulation phases are

not necessarily synchronized with each other(Fig. 7). Interconnecting these two laminaeare a dense continuous network of branchinganastomosing elastic fibers, in which incom-plete fragmental elastic laminae occasionallyoccur (Fig. 7). Tunnel-like compartments,although not as clearly seen as those in theaorta, extend into the arterial wall in the samehelical direction (Fig. 7). The adventitialelastic tissue is poorly developed as comparedwith that in the aorta and consists of a sparsenetwork of fine curly elastic fibers, throughwhich the subjacent EEL can be easily seen(Fig. 9). The fibe rs are clearly joined w iththe surface of the EEL.

DISCUSSIONThe overall tridimensional architecture ofthe elastic tissue in the rat aorta (elastic typeartery) and femoral artery (muscular typeartery) has been studied by scanning electronmicroscopy after hot-formic acid extraction

followed by freeze-drying method. Thegeneral organization of the elastic tissue wasnot considerably altered by the formic acidtreatment, as confirmed by the comparison onthin sections from intact and extracted tissues.Previous TEM studies18'101 have suggestedthat the arterial elastic tissue may have a con-tinuous network throughout the vascular walls.This suggestion remains speculative, however,since one can hardly know the overall archi-tecture of such a spatially intricate structureas the elastic tissue only by a two-dimensionalplane of section in which it often appears inthe form of isolated fragments. The presentSEM study has clearly demonstrated that thearterial elastic tissue actually makes a com-pletely continuous network throughout thevascular walls from its intimal to adventitialelement, regardless of the considerable dif-ferences in its overall structural organizationbetween the two distinct types of arteries ex-amined. This finding strongly supports theidea13'191 that such a completely continuousnetwork of the arterial elastic tissue, surround-


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Tridimensional Architecture of Arterial Elastic Tissue 43ing compartments in which medial smoothmuscle cells and collagen fibers are enclosed,can function as a unit, distributing the intra-luminar distension pressure uniformly aroundthe whole circumference of the vascular wallsand the reby counterb alancing the large pulsatileintraluminar pressure of the vessels.

By tridimensional observations, tunnel-likecompartments, extending into the vascularwalls in the same helical direction, have for thefirst time been demonstrated clearly in theaorta and less clearly in the femoral artery.When correlating the SEM images with TEMmicrographs in which the elastic tissue oftenseems to encircle the individual smooth musclecell, it is obvious that these compartmentsprobably correspond to the burrows of themedial smooth muscle cells. This findingindicates that the medial smooth muscle cellsare aligned in parallel to one another and arearranged helically around the arterial walls.

The internal elastic laminae have numerousfenestrations which are considerably differentin size, shape and structure between the twotypes of arteries examined. These structure sdo not seem to be artificial products, sincethe correlative TEM examinations of intacttissues have also shown the presence of com-parable large fenestrations, interrupted only bydot-like elastins, in the aortic IEL and simplesmall fenestrations in the IEL of the femoralarte ry. Th is finding raises the question ofwhether these fenestrations have any signifi-cant functional meaning and, if so, what func-tional role(s) they play. One interp retationis that the fenestrations are the pathwaysthrough which cellular elements and/or inter-cellular connective tissue components can passto form cell to cell junc tion and /or to establishdirect connections between the connectivetissues in adjacent com partm ents. They mayalso serve as pathways through which nutrientsubstances can diffuse from the vascularlumen into the avascular media. Con sideringthe previous TEM findings20-211 that an elec-tron-dense tracer (horseradish peroxidase)cannot penetrate into the arterial elastin matrix

leaving it entirely electron-lucent, while readilyfilling the extracellular matrix of the vascularmedia after passing through the fenestrationsof the IEL, it might be expected that thearterial elastic laminae act as a diffusionbarrier to some extent large molecules proba-bly due to the inner com pact structure. Ifthis speculation is correct, the second inter-pretation seems more likely and may wellexplain the structural diversity of the IELsbetween the aorta and femoral artery, sincethe former has a thicker wall as well as a muchmore compact medial elastic tissue than thelatter.

Ayer et al.7) examined the light microscopicappearance of the elastic tissue in the dogaorta after hot-formic acid extraction andreported that the elastic laminae are not solidsheet-like structures, but are composed ofmultiple fine elastic bands which run indifferent directions without order and repeated-ly split and fuse with each other, resulting inthe formation of tightly weaved mesh-likeelastic laminae. A similar fibrous substruc -ture of aortic elastic laminae has been demon-strated by Hart et al.n) who examined theSEM appearance of the elastic tissue in theyoung swine aorta using guanidine-NaOHextraction technique. According to theseauthors, the aortic elastic laminae consist ofcompletely fibrous elastins running alternatelyin different directions in successive laminae.In the present study no such fibrous sub-strcture could be demonstrated in the ratao rtic elastic lamin ae. It is no t possible atpresent to determine whether these structuraldifferences between the aortic elastic laminaeof various animals examined to date is at-tributed to the interspecies variations, dif-ferent developmental stages of animals ex-amined or different extraction procedures used.In view of the fact, however, that Carnes etal.14) have demonstrated, using the same ex-traction technique as used by Hart et al.,

22)

that the aortic elastic laminae of the humanadult consist of solid sheet-like structure whichis very similar to those of the rat described in



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this study, it might be proposed that thegeneralization about structural details of thearterial elastic tissue cannot be made withoutregard for its animal source rather than theextraction technique employed.Acknowledgment. This work was supported byGr ant s (No . 107003, N o. 57770022) from the Ministryof Education, Science and Culture, Japan.

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Artery SCM