SMITHSONIAN MISCELLANEOUS COLLECTIONSVOLUME 72, NUMBER 10
THE CIRCULATORY SYSTEM IN BONEWith Six Plates
BYJ. S. FOOTE, M. D.
(Publication 2652)
CITY OF WASHINGTONPUBLISHED BY THE SMITHSONIAN INSTITUTIONAUGUST 20, 1921
BALTIMORE, MD., U. S. A.
THE CIRCULATORY SYSTEM IN BONEBy J. S. FOOTE, M. D. 'Professor of Pathology, Medical Department of Creighton University,Omaha, Islebraska(With 6 Plates)INTRODUCTIONThis article on the circulatory system in bone is the result of acontinued study of the comparative histology of bone published in amonograph entitled " A Contribution to the Comparative Histologyof the Femur," Smithsonian Contributions to Knowledge, Vol. 35,No. 3, 1916.In that monograph were described the structural bone types andthe type combinations as they were observed in cross sections of thefemora of various animals from amphibians to and including man.^The circulation within the bone substance was not seen at that time,as cross sections do not show it properly.In 1919 a casual preparation of a tangential section of the femurof a domestic turkey disclosed a very remarkable circulation in thebone substance and it was this disclosure that led to further examina-tion of tangential sections of the bones of different animals, the draw-ings and descriptions of which are here presented.Later (1919-20) the structure of and circulation in the bone of thefish, as seen in the Mascalonge, Esox, were studied, compared withithe bone types of later vertebrate animals and added to the list ofbones examined.THE CIRCULATORY SYSTEM IN BONEThe circulatory system in bone, as usually described, is limited tothe blood vessels of periosteal membranes, medullary canals anddiploe of long and cranial bones respectively, little being known aboutthe circulation within the bone substance itself.The circulation described in this article is situated in the bonesubstance of the mandible and cranial bones of the fish, Mascalonge,Esox, in the walls of the long bones of the amphibian, reptile, bird,
* Number of sections of femora described and drawn in the monograph, 440.Smithsonian Miscellaneous Collections, Vol. 72, No. 10
2 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 72
bat, Other mammals and man, in the cranial bones of man, in the innerwall of the 9th rib and in the infra- and supra-spinous fossae of thescapula of man. The blood supply of the lower jaw and cranial bonesof the fish is derived from the dermal vessels which enter the boneat various points and assume parallel positions in the bone substance,while the blood supply of the long bones of the higher vertebratescomes from two sources, viz. the periosteal vessels which send offmany small branches into the bone through entering canals (canalsof Volkmann and other canals), and the medullary arteries whichpass obliquely through the walls of the shafts into the medullarycanals where they divide into ascending and descending branchesfrom which small vessels are sent off into the walls of the bones andhere become continuous with the vessels from the periosteum.The blood supply of the flat bones, such as the cranial, is derivedfrom the vessels of the pericranial and endocranial membranes whichsend off branches into the outer and inner tables of these bones com-municating by way of the central medullary diploe.From a study of a large number of bone sections ^ there are foundto be three structural types and various type combinations ' whichenter into the formation of bone : these are the first, composed oflamellae ; the second, composed of laminae ; and the third, composedof Haversian systems. These three types are combined in variousproportions in the bones of different animals. The circulationswhich are found to be present in the different types of bone alsopresent variations which are sufficiently distinctive in character toform two circulatory types, viz., the branching, and the plexiform.The branching type, composed of tree-like branches, is found in thefirst type bones, the plexiform, composed of small, large and irregu-larly shaped meshes enclosed by small vessels, is found in the secondand third type bones, while combinations of the branching and plexi-form circulations are present in structural type combinations.In the demonstration of the circulations some difffculty arises inthe preparation of the bone slides. In small animals like the frogsor other animals of the same size it is practically impossible sincethe long bones are almost always round and tangential sections ofthem are necessarily flat. In large animals the long bones have flatareas of sufficient extent to make satisfactory sHdes.In the preparation of bone sections for the purpose of showing thecirculation, a flat surface of bone is selected and as large a piece as
^ Number of sections of bones examined up to the present, 1000.
^ A Contribution to the Comparative Histology of the Femur, by J. S. Foote,M. D., Smithsonian Contr. to Know!., Vol. 35, No. 3, 1916.
NO. lO THE CIRCULATORY SYSTEM IN BONE FOOTE 3possible is sawed out, tangential to the diameter of the bone, andground down to a suitable thinness which is determined by the ap-pearance of the circulation.It is not the thinnest possible section, measured in microiis, thatis most desirable, but one of sufficient clearness to show the circula-tion. During the grinding process it is necessary to examine thesection at short intervals in order to ascertain just when to terminatethe process.The following sections taken from the bone of fish, amphibian,reptile, bird, mammal, and man have been studied, described, anddrawn for the purpose of showing the structure and the circulationwhich belongs to it.CROSS AND TANGENTIAL SECTIONS OF THE LOWER JAW ANDTANGENTIAL SECTION OF THE CRANIAL BONE OF THE MAS-CALONGE, ESOX, A FISH OF WISCONSIN WATERSCROSS SECTION OF A PORTION OF THE LOWER JAWPl. I, Fig. iaThe section is composed of parallel disks of bone substance situatedbetween vascular channels or clefts. The bone substance does notshow the presence of lacunae with their canaliculi. Very minuteparallel canaliculi extend across the disks from one channel or cleftto another. A wave effect is given to the section by the undulatingforms of the clefts. This arrangement of channels in the bone sub-stance produces a very fine channel circulation. At short intervalswithin the clefts, as at C, figure i, plate i, may be seen small objectsfrom which radiate minute canaliculi presenting the appearance ofthe canaliculi radiating from their lacunae, but these are in the vas-cular clefts and not in the bone substance.TANGENTIAL SECTION OF A CRANIAL BONE OF THE MASCALONGEPl. I, Fig. ibIn this section are seen parallel rows of objects of various shapessituated in the bone substance. Some of them are circular with darkcrescents on one side, while others are very irregular in shape. Nocanaliculi extending outward from them can be seen. For thisreason they cannot be lacunae in the bone substance, as osteoblastsoccupying such lacunae would be without a blood supply. On ac-count of their general circular character these objects appear to bedifferent sections of the vascular clefts of the bone and if any bone-producing cells are present they must be within the vascular clefts.
4 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 'J2.CROSS SECTION OF ANOTHER PORTION OF THE LOWER JAW OF THE MAS-CALONGE SHOWING THE EARLY DIFFERENTIATIONS OFHAVERSIAN SYSTEMSPl. I, Fig. 2These are small vascular canals surrounded by clear areas—insome instances lamellated, in others, homogeneous. Between thevascular canals is the bone substance with very fine channels. Thevascular canals with surrounding clear areas become Haversian sys-.terns as vascular differentiation progresses. This early form ofHaversian differentiation has a wide distribution since it is found inbone sections from fish to and including man. It is much more prom-inent in the lower orders of vertebrates than in the higher. Thustwo early phases of the circulation are found in the bone of themascalonge, viz., the channeled and early Haversian differentiation.
TANGENTIAL SECTION OF THE INNER RIDGE OF THE LOWER JAW OFTHE MASCALONGE SHOWING THE BLOOD VESSELSPl. I, Fig. 3The blood vessels vary in size. They are parallel with each other.Some are branching. Around the outside of their delicate connectivetissue walls are seen fine plexuses of nerves. Between the vesselsis seen a fine channeled bone substance without lacunae.CROSS AND LONGITUDINAL SECTIONS OF THE FEMUR OF AMEDIUM SIZED BULLFROG, RANA CATESBEIANA(The large, medium sized and small bullfrogs have different degrees of bonedifferentiation.) *CROSS SECTION SHOWING THE STRUCTUREPl. I, Fig. 4The type of bone is an early first. The inner wall is composed ofbone substance in which are radiating, vascular, bush-like channelsextending from the external to the internal circumferential lamellaeand between which are round or oval lacunae with short branchingcanaliculi embedded in the bone substance and communicating withthe bush-like radiations by means of their canaliculi. The bush-likevascular radiations appear to be segmented in some instances dueto their oblique positions and the plane of the cross section. In theouter wall these radiating channels are absent and the bone is com-posed of lamellae with oval lacunae and radiating canaliculi.
—— ^
* Idem.
NO. 10 THE CIRCULATORY SYSTEM IN BONE—FOOTE 5LONGITUDINAL SECTION OF THE SAME FEMUR SHOWING THECIRCULATIONPl. I, Fig. 5The oblique entering canals in the shafts of the femora of bullfrogs, for the passage of the medullary arteries, are found in the boneof the large and medium sized but not in the small animals. As thefemur of the frog is small and round the circulation in a tangentialsection could not be seen. The general plan, however, is shown in alongitudinal section of the inner wall as represented in figure 5,plate I. The letter C is placed at the center of the shaft. In this wallare two sets of six or seven oblique vascular canals entering the shaftfrom the periosteal surface and united in such a manner as to formslanting m-shaped converging loops. These loops, beginning nearthe extremities of the shaft, converge toward the lineal center andmedullary surface. From these loops and their stems minute can-aliculi are sent ofif into the bone substance where they communicatewith the lacunae. Between the two sets of converging loops are shortsegments of loops extending across the wall transversely. In theouter wall the loops are not seen in longitudinal section nor are theradiating vascular channels seen in the cross section of this wall.CROSS AND TANGENTIAL SECTIONS OF THE FEMUR OF THEREPTILE, ALLIGATOR MISSISSIPPIENSISCROSS SECTION SHOWING THE STRUCTUREPl. I, Fig. 6This section is composed of three wide, concentric rings of incom-pletely differentiated Haversian systems alternating with two narrow,concentric laminae. The vascular canals surrounded by clear areassimilar to those seen in the bone of the fish are early forms ofHaversian systems. The laminae are more advanced in differentia-tion than the Haversian systems. The bone, as a whole, shows anearly second and third type structure.TANGENTIAL SECTION OF THE SAME FEMUR, SHOWING THECIRCULATIONPl. I, Fig. 7The circulation is in the form of a vascular plexus. The sectionis situated below the periosteal surface near the posterior ridge.Several entering canals, without surrounding lamellae, are seen in
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cross section in the bone substance through which periosteal vesselspass into the bone. The vascular plexus is very extensive and hasa general longitudinal direction. The meshes are irregular in sizeand shape. In some portions of the section vascular expansions arefound. The blood vessels are round and occupy similarly shapedchannels in the bone substance. They are composed of very thinconnective tissue walls, without smooth muscle, and are striatedspirally and longitudinally. The exact purpose of the vascular ex-pansions is not clearly understood. They are found too frequentlyto be accidental, and, as will be noted later, are more prominent inthe branching than in the plexiform types of circulation. They mayhave an important physical value.CROSS AND TANGENTIAL SECTIONS OF A SECOND TYPE BONEOF BIRDS AS SEEN IN THE FEMUR OF A DOMESTICTURKEY, MELEAGRIS GALLOPAVOCROSS SECTION SHOWING THE STRUCTUREPl. I, Fig. 8The section is composed of concentric laminae separated andcrossed by vascular canals. The wall of the bone is divided intonearly equal segments by large radiating canals extending from themedullary canal to the periosteal surface. From these canals aresent off lateral, small, parallel canals which divide the wall of thebone into laminae. The laminae are interrupted in the anterior walland posterior ridge by incompletely differentiated Haversian systems.It was the femur of the turkey which first called attention to thevariations in structure and circulation.
TANGENTIAL SECTION OF A FEMUR OF THE TURKEY, SHOWINGCIRCULATIONPl. I, Fig. 9This section consists of a very rich, small-meshed plexus of vesselssituated between the laminae and having a general longitudinal direc-tion. In the central portion of the section two plexuses can be seen,one above the other, with a lamina of bone between them. This isone of the most extensive circulations observed in long bones andwith such a blood supply as is here shown, this becomes a vascularorgan of great importance.
NO. 10 THE CIRCULATORY SYSTEM IN BONEi FOOTE 7RECONSTRUCTION OF A SECOND TYPE BONE WITH ITS INTER-LAMINAR CIRCULATIONPl. 2, Fig. ioThis figure shows a reconstruction of a second type bone with itscirculation. The drawing represents three concentric laminae withtwo interlaminar plexuses of blood vessels. The vessels are uniformin size, composed of thin connective tissue walls and the vascularexpansions are not at all prominent. It is difficult to understand whysuch a rich blood supply should be required in bone for its nutrition.CROSS AND TANGENTIAL SECTIONS OF AN EARLY DIFFERENTI-ATION OF A THIRD TYPE BONE IN BIRDS AS SEEN IN THEFEMUR OF A TURKEY BUZZARD, CATHARTESAURA SEPTENTRIONALISCROSS SECTION SHOWING THE STRUCTUREPl. 2, Fig. iiThis bone is more advanced in differentiation than that of thedomestic turkey since it is composed of third type structural boneunits instead of the second. These units are enclosed between theexternal and internal circumferential lamellae and form nearly thewhole bone structure.TANGENTIAL SECTION OF THE FEMUR OF THE SAME ANIMAL SHOWINGTHE CIRCULATIONPl. 2, Fig. i2The meshes of the circulatory plexus are longer and enclose largerbone areas than those seen in the femur of the turkey. The vascularexpansions are not as prominent as they are in some of the otherbones, but may be seen here and there. A general plexiform plan ofcirculation is evident, but an elongation of the meshes in the centralportion shows a slight variation in the circulatory distribution.TANGENTIAL SECTION OF THE FEMUR OF A DOMESTICCHICKEN, CALLUSPl. 2, Fig. 13The type of structure is a first and early third. Several enteringcanals without surrounding lamellae are present. The circulationappears as a rich plexus of small blood vessels coming off from acentral vessel which extends lengthwise of the section. The meshesof the plexus are small, round, oval or irregular in shape and thelacunae of the bone substance are round or oval with short, branchingcanaliculi.
8 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 72TANGENTIAL SECTION OF THE FEMUR OF A PRAIRIE CHICKEN,TYMPANUCHUS AMERICANUS, SHOWING THECIRCULATIONPl. 2. Fig. 14The type of bone is first. A few entering vascular canals, withoutsurrounding lamellae, are seen in the bone substance. The circula-tion is a rich plexus of blood vessels with small, round and irregularlyshaped meshes. It is situated nearer the periosteal than the medullarysurface. The lacunae of the bone substance are round or oval andhave short bushy canaliculi.TANGENTIAL SECTION OF THE FEMUR OF A DOMESTIC DUCK,ANAS DOMESTICA, SHOWING THE CIRCULATIONPl. 2, Fig. 15The type of bone is an early second. The section has two richplexuses of blood vessels, one above the other, with bone substancebetween them. The meshes are quite regular in form and somewhatlarger than those found in the other birds examined. Here and thereare seen entering vascular canals without surrounding lamellae. Thelacunae of the bone substance are round or oval with short bushycanaliculi.CROSS AND TANGENTIAL SECTIONS OF THE FEMUR OF AFRUIT BAT, PTEROPUS (CELEBES)CROSS SECTION SHOWING THE STRUCTUREPl. 2, Fig. 16The section is composed of a wide central ring of lamellae per-forated in the inner wall by a few vascular canals extending length-wise of the bone. Internal circumferential lamellae surround themedullary canal and poorly differentiated external lamellae surroundthe section. The lacunae are oval with straight canaliculi.
TANGENTIAL SECTION OF THE SAME FEMUR SHOWING THECIRCULATIONPl. 2, Fig. 17In this section are seen the vascular canals of the inner wall extend-ing from above downward and inward. The canals are parallel witheach other and some of them are branched. They were absent in theouter wall.
NO. lO THE CIRCULATORY SYSTEM IN BONE^ FOOTE 9CROSS AND TANGENTIAL SECTIONS OF A SECOND TYPE BONEIN MAMMALS AS SEEN IN THE FEMUR OF A LAMB, OVISCROSS SECTION SHOWING THE STRUCTUREPl. 2, Fig. i8The section is composed of concentric laminae which are more com-pletely differentiated than they are in birds. Here and there thelaminae are interrupted by Haversian systems of a late differentiationand the concentric canals between the laminae are widened at inter-vals and around them are incompletely differentiated lamellae form-ing an early aberrant type of Haversian system. The posterior ridgeis composed of Haversian systems of a late differentiation.TANGENTIAL SECTION OF THE FEMUR OF THE SAME ANIMAL SHOWINGTHE CIRCULATIONPl. 2, Fig. 19The circulatory plan of arrangement in this bone is not preciselylike that observed in the second type bone in birds. While it is plexi-form in character there is about it more or less irregularity in distri-bution approaching the branching type of circulation. Near thesides of the drawing the plexus has a long mesh ; while in the centralportion it has more of a branching character. The vascular expan-sion seen in the center of the drawing gives the impression of adistributing point in the circulation. A few entering vascular canalsare seen.CROSS AND • TANGENTIAL SECTIONS OF ANOTHER SECONDTYPE BONE IN MAMMALS AS SEEN IN THE FEMUR OFTHE MEXICAN BURROCROSS SECTION SHOWING STRUCTUREPl. 2, Fig. 20The section is composed of concentric laminae interrupted byHaversian systems of different degrees of differentiation. The struc-ture is similar to that seen in the femur of the lamb and a largenumber of other mammals which have the same type bone.TANGENTIAL SECTION OF THE FEMUR OF THE SAME ANIMAL,SHOWING THE CIRCULATIONPl. 2, Fig. 21The type is plexiform and the meshes of the plexus are much moreregular in shape than those seen in the femur of the lamb. There isno evidence of a branching character. The vascular expansions arenot as prominent as they were in the femur of the lamb.
10 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 72TANGENTIAL SECTION OF THE FEMUR OF AN ELK, ALCESAMERICANUS, SHOWING THE CIRCULATIONPl. 3, Fig. 22The type of bone is second. Several perforations in the bone sub-stance for the passage of blood vessels are present. Some of themare surrounded by enclosing lamellae and some are not (Volkmann'scanals). The circulation is an extensive plexus of blood vessels withround and irregularly shaped meshes. It has a general directionlengthwise of the bone.TANGENTIAL SECTION OF THE FEMUR OF A BELGIAN HARE,LEPUS, SHOWING THE CIRCULATIONPl. 3, Fig. 23The type of bone is an early second and third. Entering vascularcanals through which blood vessels are seen to pass and ramify inthe bone substance are present in the central portion of the section.The canals are not surrounded by lamellae. The circulation is a com-bination of a branching and plexiform distribution. The vascularexpansions are prominent. One is seen in a vessel shortly afterentering the bone. It is a matter of observation in bone circulationsthat the type of circulation varies with the type of structure.TANGENTIAL SECTION OF THE FEMUR OF A BULLDOG,SHOWING THE CIRCULATIONPl. 3, Fig. 24The type of bone is second and third. Entering vascular canals,without enclosing lamellae, are seen in the bone substance throughwhich blood vessels are passing. The circulation is a dense branchingand plexiform combination. The vessels are small in diameter, fre-quently branching, the union of their branches producing a plexiformefifect.CROSS AND TANGENTIAL SECTIONS OF THE FEMUR OF AMONKEY, MACACA RHESUSCROSS SECTION SHOWING THE STRUCTUREPl. 3, Fig. 25The type of bone is first and third. The section is composed oflamellae interrupted by Haversian systems of early and late diiTer-entiations. Crescents of late Haversian differentiation are foundbordering upon the medullary canal in the anterior inner and pos-terior outer wall. The lacunae of the bone are long with straightcanaliculi. The principal structure is lamellar and the type is muchmore first than third.
NO. lO THE CIRCULATORY SYSTEM IN BONE: FOOTE IITANGENTIAL SECTION OF THE SAME FEMUR, SHOWING THECIRCULATIONPl. 3, Fig. 26A few entering vascular canals without surrounding lamellae arepresent. The circulation is a dense branching type which, here andthere, presents a slight appearance of the plexiform distribution. Theblood vessels are large and trunk-like in places and a very few vas-cular expansions are present.CROSS AND TANGENTIAL SECTIONS OF THE FEMUR OF A9 MONTHS' HUMAN WHITE FETUSCROSS SECTION SHOWING THE STRUCTUREPl. 3, Fig. 27The section is composed of short laminae with central canals widen-ing and shortening until they are transformed into Haversian sys-tems. External circumferential lamellae surround the section (pos-terior wall excepted) and directly underneath the lamellae is a rowof advanced differentiations of Haversian systems. The medullarycanal is small, irregular in shape and situated in the anterior halfof the section. The posterior wall is composed of Haversian systemsof advanced differentiations and in the mid line where the walls ofthe bone unite is a narrow radiating layer of bone substance whichdisappears as complete union takes place.TANGENTIAL SECTION OF THE SAME FEMUR SHOWING THECIRCULATIONPl. 3, Fig. 28The circulation is plexiform in type, the general direction of whichis longitudinal and slightly oblique. The vessels forming the plexushave short branches which seem to disappear in the bone substancewithin the meshes. Vascular expansions are present, one beingshown in the left central portion of the figure.CROSS AND TANGENTIAL SECTIONS OF THE FEMUR OF AWHITE CHILD 9 YEARS OLDCROSS SECTION SHOWING THE STRUCTUREPl. 3, Fig. 29The type of bone is first and third. Around the periphery of thesection is a wide crescent shaped band of lamellae enclosing numerousvascular canals of the earliest Haversian differentiation, such as were
12 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 'J2.
observed in the bone of the fish, plate i, figure 2. Around the medul-lary canal are the internal circumferential lamellae forming an enclos-ing ring of irregular widths. Within this ring are also foundvascular canals of early Haversian differentiation extending longi-tudinally. Between the external and internal lamellae abovedescribed, is a ring of Haversian systems of late differentiation,deficient in the anterior wall and increasing in width in the outerlateral wall as it reaches the posterior ridge. The lacunae are longand narrow with straight canaliculi.TANGENTIAL SECTION OF THE SAME FEMUR SHOWING THECIRCULATIONPl. 3, Fig. 30Entering canals with and without enclosing lamellae are of fre-quent occurrence. The circulation is a combination of the branchingand plexiform types. The central portion is branching and thelateral, plexiform, vascular expansions are not as prominent as theyare in many other sections. The section shows the circulatory com-bination of type conforming to the structural type combination.CROSS AND TANGENTIAL SECTIONS OF THE FEMUR OF ADULTMAN, A WHITE MALECROSS SECTION SHOWING THE STRUCTUREPl. 4. Fig. 31The bone is third type in differentiation with the exception of aportion of the anterior wall where the remains of first type bone arefound. The section is composed of completely differentiated Haver-sian systems, some of which are senile. The external circumferentiallamellae are fragmentary, while the internal are complete.TANGENTIAL SECTION OF THE SAME FEML% SHOWING THECIRCULATIONPl. 4, Fig. 32The type of circulation is plexiform with wide, irregularly shapedmeshes. Entering vascular canals surrounded by lamellae are seenhere and there in the section. Vascular expansions are prominent.This section is taken from the bone represented in plate 4, figure 31,near the periosteal surface of the left side of the drawing and nearthe posterior ridge. It is difficult to think of the circulation as shownin plate 4, figure 32, as belonging to that locality.
NO. 10 THE CIRCULATORY SYSTEM IN BONE—FOOTE I3TANGENTIAL SECTION OF THE FEMUR OF MAN, A WHITE MALE,SHOWING CIRCULATIONPl. 4, Fig. 33The type of bone is first and third. Numerous entering vascularcanals with and without enclosing lamellae are present. The circula-tion is a dense branching and plexiform distribution of blood vesselswith small meshes of various shapes. Vascular expansions arenumerous and large. The lacunae of the bone substance are round,oval, and long and narrow with the canaliculi which belongs to eachdegree of differentiation. The density of the circulation varies indifferent bones of the same structural type and also in bones ofdifferent type combinations.
TANGENTIAL SECTION OF THE FEMUR OF MAN, A WHITE MALE,SHOWING THE CIRCULATIONPl. 4, Fig. 34The type of bone is first and third. The type of circulation isbranching, changing to plexiform. Entering canals, for the mostpart without enclosing lamellae, are few in number in this section.The circulation shown in the drawing is situated in the externallamellae which encloses the internal third type differentiation. It isa large branch dividing into many small ones which, by uniting, forma plexiform distribution.
TANGENTIAL SECTION OF THE FEMUR OF MAN, A WHITE MALE,AGE 50, WHO DIED OF PULMONARY TUBERCULOSISPl. 4, Fig. 35The type of bone is third. The type of circulation is essentiallybranching although a coarsely plexiform arrangement can be distin-guished. Entering canals with and without enclosing lamellae areseen in the bone substance. The blood vessels are irregular in sizeand shape and show varicose enlargements very frequently. Whetheror not this varicose condition and irregularity in the circulation inbone are indices of similar changes in the general circulation cannotbe told ; but they may be thought of in connection with the pathologi-cal condition present in this individual.
14 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 72THE CIRCULATION IN FLAT BONESCROSS, LONGITUDINAL, AND TANGENTIAL SECTIONS OF AHUMAN FRONTAL BONECROSS SECTION SHOWING THE STRUCTUREPl. 4, Fig. 2^The bone is composed of outer and inner tables united by a centralcancellous diploe. The two tables are composed of first type boneenclosing a few Haversian systems in cross section and a few shortsegments of blood vessels. The diploe is a coarse, cancellous bonewith large, small, and irregularly shaped cavities enclosed by firsttype bone walls. The walls are composed of lamellae in whichHaversian systems are seen in cross section. This section was takenfrom the vertical portion of the frontal bone.LONGITUDINAL SECTION OF THE SAME FRONTAL BONE, SHOWING THESTRUCTUREVu 4, Fig. 37This section has practically the same structure as the cross section,as may be seen by comparing the drawings. This section is cutat right angles to that seen in plate 4, figure 36. It is taken from thesame region, and Haversian systems, in cross section, are found inboth situations. The Haversian systems therefore run at right anglesto each other, which can hardly be accounted for on mechanicalgrounds.TANGENTIAL SECTION OF THE OUTER TABLE OF THE SAME FRONTALBONE TAKEN FROM THE SAME REGION AS FIGURE 36, PLATE 4,SHOWING THE CIRCULATIONPl. 4 Fig. 38The section is situated nearer the external surface of the bone thanthe diploe. Numerous entering canals with and without enclosinglamellae are found in the bone substance. The circulation is branch-ing in type. The vascular expansions are large and numerous andappear to form physical centers of distribution. The blood vesselsare relatively large and frequently branch.ENTERING VASCULAR CANALS OF THE OUTER TABLE OF THEFRONTAL BONEPl. 5, Fig. 39There are two forms, the one at the left in the drawing withoutenclosing lamellae (Volkmann's canals), and the one at the rightwith enclosing lamellae. The Volkmann's canals are smaller than
NO. 10 THE CIRCULATORY SYSTEM IN BONE FOOTE 1
5
the Others. As soon as the blood vessels pass through the externalsurface of the bone they send off branches into the planes of theirdivisions and form the branching distributions there.TANGENTIAL SECTION OF THE INNER TABLE OF THE SAME FRONTALBONE, SHOWING THE CIRCULATIONPl. 5, Fig. 40In this section the bone is perforated by numerous entering canalswith and without enclosing lamellae. The blood vessels from thecerebral surface enter the bone by these canals and find their way tothe diploe. The circulation within the bone is branching in type andsituated nearer the cerebral surface than the diploe. Many vascularexpansions are present with their incoming and outgoing vessels.TANGENTIAL SECTION OF THE OUTER TABLE OF A HUMANPARIETAL BONE, SHOWING THE CIRCULATIONPl. 5, Fig. 41The section is taken from the central portion of the bone. Thetype of bone is first. Entering vascular canals surrounded by lamellaeare numerous. The circulation is branching in type. Vascular ex-pansions are large and numerous. Those in the center give the im-pression of distributing points in the circulation.TANGENTIAL SECTION OF THE INNER TABLE OF THE SAME PARIETALBONE SHOWING THE CIRCULATIONPl. 5, Fig. 42The section is situated nearer the cerebral surface than the diploe.Entering vascular canals with enclosing lamellae are numerous. Thecirculation is branching in type and not as dense as that of the outertable. The vascular expansions are many and large. The type ofbone is first.TANGENTIAL SECTION OF THE SQUAMOUS PORTION OF THETEMPORAL BONE OF MAN, SHOWING THE CIRCULATIONPl. 5, Fig. 43The type of bone is first. Entering canals with and without en-closing lamellae are present. The circulation is branching in typeand the vascular expansions are large and very numerous. The ex-pansions vary in size and frequency of occurrence in different sec-tions. In some instances they are very small and few in number, inothers, large and numerous, and they are much more prominent in the
l6 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 72branching than in the plexiform type of circulation. They areespecially prominent in this section.TANGENTIAL SECTION OF THE OUTER TABLE OF A HUMANOCCIPITAL BONE, SHOWING THE CIRCULATIONPl. 5, Fig. 44The section is taken a short distance above the foramen magnum.The circulation is a dense branching type situated near the externalsurface of the bone. There are many vascular expansions fromwhich branching vessels take their departure. Entering canals withand without surrounding lamellae are present in the first type bonesubstance.TANGENTIAL SECTION OF THE INNER TABLE OF THE SAME OCCIPITALBONE, SHOWING THE CIRCULATIONPl. 5, Fig. 45The type of bone is first. Entering canals with and without sur-rounding lamellae are numerous. The section is situated near thecerebral surface. The circulation is branching in type and verydense in character. Large branches extend in different directionsand from these, small branches are sent ofif into the bone substance.The vascular expansions are not as numerous as those in the outertable, figure 44.TWO VASCULAR EXPANSIONS AS THEY WERE SEEN IN THE OUTERTABLE OF THE OCCIPITAL BONEPl. 5, Fig. 46The vascular expansions are observed in all branching and inmany sections of the plexiform type of circulation. They are nearlyalways filled with fat globules with dark, wide contours which areso closely faceted together that they completely occupy the expansioncavities. This would, of course, block the circulation if it existedin the living bone. The condition was misleading in significanceuntil it was noticed that the fat globules were found in ground sec-tions and not in thin unground bone plates ; so that they are probablyproduced by the melting heat of friction during the grinding processand fill the expansions. The ex]:)ansions probably have a physicalvalue as distributing centers in the circulation or they may be forthe purpose of establishing and maintaining a circulatory equilibriumin bone.
NO. lO THE CIRCULATORY SYSTEM IN BONE—FOOTE 1
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TANGENTIAL SECTION OF A HUMAN INFERIOR MAXILLA,SHOWING THE CIRCULATIONPl. s, Fig. 47The section is taken from the bone just in front of and below theleft central incisor tooth. The type of bone is first. Entering canalswith and without lamellae are present. The circulation is a branch-ing plexiform type having a slanting direction from above downwardand forward. The meshes are long and irregular in shape. Vascularexpansions are numerous.TANGENTIAL SECTION OF THE INFRA-SPINOUS FOSSA OF AHUMAN SCAPULA, SHOWING THE CIRCULATIONPl. 6, Fig. 48The type of bone is first with here and there an Haversian system.A few entering canals with enclosing lamellae are seen in the section.The circulation is a branching and plexiform type, the former pre-dominating. Vascular expansions are prominent. The one in thecenter of the drawing suggests a distributing center.TANGENTIAL SECTION OF THE SUPRA-SPINOUS FOSSA OF THE SAMESCAPULA, SHOWING THE CIRCULATIONPl. 6, Fig. 49The type of bone is first. A few entering canals with and withoutsurrounding lamellae are present. The circulation is branching intype with a few vascular expansions. It takes an oblique directionfrom above downwards and toward the vertebral border,CROSS AND TANGENTIAL SECTIONS OF THE 9TH RIB OF ADULTMAN, MALE WHITECROSS SECTION SHOWING THE STRUCTUREPl. 6, Fig. 50This is a third type bone composed of Haversian systems of a latedegree of differentiation. The systems extend lengthwise of the riband enclose a cancellous center.TANGENTIAL SECTION OF THE INNER WALL OF THE SAME RIB,SHOWING THE CIRCULATIONPl. 6, Fig. 51The section is taken from the posterior third of the bone. Thecirculation is an elongated plexus. In the center of the section is avascular expansion which suggests a center of distribution for theblood vessels.
l8 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 72DEVELOPMENTAL ADVANCES IN THE CIRCULATIONDETERMINE THE STRUCTURAL TYPES OF BONEIt is generally supposed that bone is preeminently mechanical infunction on account of its position in the body and its rigid character.It forms the skeleton of the animal body, supports its weight, givesattachment to muscles by means of which locomotion is possible,serves as a framework upon which the viscera are hung, affords pro-tection and gives efficiency to the laboratory of chemical activitiesconstantly in operation during life. It is chiefly for these reasonsthat we attribute a mechanical function to bone. This thought isfurther strengthened by the microscopic structure so familiar to useither from personal observation or from text books of histology,in both of which bone is represented, usually, as composed of Haver-sian systems.There are however, as shown before, three structural types ofbone, the first, second, and third.The first type is composed of bone substance or lamellae, thesecond of laminae which are produced by a vascular separation oflamellae into parallel divisions, and the third, of Haversian systemswhich are produced by arranging lamellae around small central vas-cular canals called Haversian canals. The Haversian system, there-fore, is the most complex and highly organized bone unit. The typesof structure follow the advancing changes in the circulation, sincethe second type bone is not recognizable until the first has been separ-ated into laminae by parallel vascular canals. There are two generaltypes of circulation, the branching and the plexiform, each one givingan individual character to the type of bone it produces. Bone de-rived from connective tissue membranes retains the branching circu-lation of those membranes, while bone derived from cartilage hasthe plexiform circulation.In going from a branching to a plexiform type of circulation, thetype of bone advances from the first to the second or third. Theblood supply in a plexiform circulation is greater in volume than itis in a branching circulation, for the reason that there are more bloodvessels in a given area in the former than in the latter. This in-creased blood supply adds an increased physiological value to thebone units of structure and is the foundation of advancement intissue values : so that blood supply is determined by the extent, planof distribution, or type of circulation and the type of tissue, phys-iologically considered, by the blood supplv, or in this particularinstance, the type of bone is determined by the type of circulation.
NO. lO THE CIRCULATORY SYSTEM IN BONE FOOTE IQTHE STRUCTURAL UNITS OF BONE—FIRST, SECOND, ANDTHIRD, OR LAMELLAE, LAMINAE, AND HAVERSIANSYSTEMS—ARE NOT ESSENTIALLY MECHANICALIf all bones were Haversian system bones, or, if there was any onebone which always has Haversian systems as the predominatingstructural units, no matter in what individual it was found, we mightbe convinced that their constant presence was sufficient evidence ofa mechanical function. But when we know that there are three boneunits of structure and that no one of them is constantly present inbones of different animals as the only unit, and not even in bones ofindividuals of the same birth,^ the idea of a purely mechanical func-tion of bone is severely shaken if not abandoned. The three units,the lamella, lamina, and Haversian system, are found in bones ofvarious animals in such great proportional and locational confusionthat their mechanical purposes disappear and we are obliged tolook further for an explanation of their strange and unexpectedoccurrences.Again, if we examine these units from a mechanical viewpointand then observe their locations in the bones of different animalswe will find that they are not always found where the same mechan-ical conditions would require them and are very often found wherethey could serve no mechanical function of any importance. Lamellaeare layers of bone substance, laminae are strata composed of lamellae,and Haversian systems are hollow cylinders composed of a variablenumber of lamellae enclosing a central canal. Of the three units,therefore, the Haversian systems offer the most mechanical serviceby construction and are the best adapted to support weight, with-stand muscular stress, and serve the general requirements of askeleton. We would, then, naturally expect to find them constantlypresent in such long bones as the femur, tibia and fibula of quad-rupeds and bipeds and generally absent from the flat bones of thehead and face. But in these respects we are disappointed. Theyare found, as a pure type, in the long bojies of only a few mammalsand are absent as predominating units in the long bones of a largenumber of mammals including the three races of man, black, yellow-brown and white.^ Haversian systems in their later degrees of dif-ferentiation are not found at all in amphibians, reptiles, birds, bats,monotremes, marsupials and many of the edentates, although thesame mechanical functions are demanded by their vocational habits.In the femur, tibia, fibula, humerus, radius, ulna, clavicle, metacarpaland metatarsal bones of man, they are present as predominating
" Idem.
° Idem.
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units in some and occur very infrequently in other individuals. Inthe flat bones of the cranium and in the irregular bones like thoseof the pelvis a few are found where it is difficult, if not impossible,to understand how they could perform any mechanical function ofany value.In the human frontal, parietal and occipital bones, a few Haver-sian systems may be found at right angles to each other ; in tliesquamous portion of the temporal bone they extend vertically ; inthe hard palate, antero-posteriorly ; in the superior and inferiormaxillae, horizontally ; in the spine of the scapula, horizontally ; inthe crest of the ilium horizontally ; and in the ribs horizontally. Inthese different situations the mechanical functions of the Haversiansystems do not seem to answer any requirement which is commonto them all. Furthermore, they are not invariably found in thesesituations and even may not be present at all. Their presence orabsence or situation within the bone is more satisfactorily explainedif we assume that developmental advances in the circulation deter-mine the types of bone. CONCLUSIONSA study of the circulations as they were observed in the foregoingslides leads one to the following conclusions
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1. That a cross section of bone gives no idea of the plan ofcirculation.2. That there are two types of circulation, the branching and theplexiform, and these are seen only in tangential sections.3. That the plan of circulation in bone derived from connectivetissue is branching; derived from cartilage, plexiform.4. That the circulation in a first type bone is branching, in thesecond and third, plexiform.5. T^hat the plexiform is a more advanced type of circulation thanthe branching and represents a later plan of vascular distributionand a more advanced degree of bone differentiation.6. That bone is a very vascular organ.7. That blood vessels are composed of extremely thin and finelystriated connective tissue walls, without smooth muscle, occupyingcanals in the bone substance.8. That vascular expansions occur in bone circulations and, bytheir positions, suggest equalizing blood pressures and uniformityin the circulation.9. That developmental advances in the circulation determine typesof bone.
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Fig. I. a. Cross section of the bone substance of the lower jaw of a Mas-calonge, Esox, showing vascular channels.I.E. Tangential section of a cranial bone of the Mascalonge, showingparallel rows of small objects in the bone substance.2. Cross section of the lower jaw of the Mascalonge, showing theearly differentiation of Haversian systems.3. Tangential section of the inner ridge of the lower jaw of Masca-longe, showing the circulation.4. Cross section of the femur of a medium sized bullfrog, Ranacatesbeiana, showing the structure.5. Longitudinal section of the femur of a medium sized bullfrog,Rana catesbeiana, showing the looped vascular canals of theinner wall. C, center of the shaft.6. Cross section of the femur of an alligator. Alligator mississippi-ensis, showing the structure.7. Tangential section of the same, showing the circulation.8. Cross section of the femur of a domestic turkey, Meleagris gallo-pavo, showing the structure.9. Tangential section of the same, showing the circulation.
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Fig. 10. Reconstruction of a second type bone with its circulation.11. Cross section of the femur of a turkey buzzard, Cathartes auraseptentrionalis, showing the structure.12. Tangential section of the same, showing the circulation.13. Tangential section of the femur of a domestic chicken, Callus, show-ing the circulation.14. Tangential section of the femur of a prairie chicken, Tympanuchusamericanus, showing the circulation.15. Tangential section of the femur of a domestic duck. Anas domestica,showing the circulation.16. Cross section of the femur of a fruit bat, Pteropus (Celebes), showingthe structure.17. Tangential section of the same, showing the circulation.18. Cross section of the femur of a lamb, Ovis, showing the structure.19. Tangential section of the same, showing the circulation.20. Cross section of the femur of a Mexican Inirro, showing the structure.21. Tangential section of the same, showing the circulation.
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Fig. 22. Tangential section of the femur of an elk, Alces americanus, showingthe circulation.23. Tangential section of the femur of a Belgian hare, Lepus, showingthe circulation.24. Tangential section of the femur of a bulldog, showing the circulation.25. Cross section of the femur of a monkey, Macaca rhesus, showing thestructure.26. Tangential section of the same, showing the circulation.27. Cross section of the femur of a 9 months fetus (human), showing thestructure.28. Tangential section of the same, showing the circulation.29. Cross section of the femur of a white child 9 years old, showing thestructure.30. Tangential section of the same, showing the circulation.
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Fig. 31. Cross section of the femur of an adult white male, showing thestructure.32. Tangential section of the same, showing the circulation.33- Tangential section of the femur of an adult white male, showing thecirculation.34. Tangential section of the femur of an adult white male, showing thecirculation.35. Tangential section of the femur of an adult white male, age So, whodied of pulmonary tuberculosis, showing the circulation.36. Cross section of a human frontal bone, showing the- structure.37. Longitudinal section of the same, showing the structure.38. Tangential section of the outer table of the same bone, showing thecirculation.
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51Fig. 48. Tangential section of the infra-spinous fossa of a human scapula,showing the circulation.49. Tangential section of the supra-spinous fossa of the same bone, show-ing the circulation.50. Cross section of the Qth rib of an adult wliite male, showing thestructure.51. Tangential section of the same bone, inner wall, showing the circula-tion.