SMITHSONIAN MISCELLANEOUS COLLECTIONSVOLUME 61, NUMBER 8
THE COMPARATIVE HISTOLOGY OFTHE FEMUR(With Three Plates)
BYDR. J. S. FOOTEProfessor of Histology and Pathology, Creighton Medical College,Omaha, Nebraska
(Publication 2232)
CITY OF WASHINGTONPUBLISHED BY THE SMITHSONIAN INSTITUTIONAUGUST 22, 1913
BALTIMORE, MD., V. S. A.
THE COMPARATIVE HISTOLOGY OF THE FEMURBy DR. J. S. FOOTEprofessor of histology and pathology, creighton medical college,omaha, nebraska(With Three Plates)The comparative study of the minute structure of the femur wasbegun by the present writer in 1909. The first report described 46microsections of the femora of as many different animals and waspublished in the Transactions of the American Microscopical Societyof April, 191 1. Following the first report and largely upon the sug-gestion of Dr. Ales Hrdlicka, Curator of the Division of PhysicalAnthropology in the United States National Museum, the writer hasextended his investigations to man of different ages and races, as wellas to many additional genera and species of animals ; and an abstractof these further studies which revealed many important and newpoints, is here presented.For the valuable material, facilities for study, and courtesiesextended, the writer is especially indebted to the Division of PhysicalAnthropology of the United States National Museum; and to theDivision of Mammals and Reptiles of the same institution ; theDepartments of Reptiles, Birds, and Mammals of the AmericanMuseum of Natural History, and the Departments of Anatomy andMedicine of the Northwestern, the Tulane, and the Creighton Uni-versities.The total number of genera and species whose femora have up tothis date been examined amounts to 400, including amphibians, rep-tiles, birds, mammals, and man. The observations have been madeon complete cross-sections of the femur at the middle of the shaft.Embryological, adolescent, adult, and senile bones of the same specieswere examined whenever it was possible, and controlling studies werealso made on other bones of the body. The drawings have been madefor the most part with the aid of the Edinger apparatus.The investigations, which are of pioneer nature, have brought outmany facts that are new to science. The existence of three types ofSmithsonian Miscellaneous Collections, Vol. 61, No. 8
2 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 6lbone, together with a number of combinations of these types, is estab-lished. They might be called the early, intermediate, and advanced,or, more definitely, the undifferentiated, laminar, and Haversian-sys-tem types. As a matter of convenience they will be referred to asthe first, the second, and the third types, respectively. They are illus-trated in plate I. They are doubtless connected intimately with vascu-lar development, and may be defined as follows
:
The first type (pi. i, fig. i) is composed of homogeneous bonesubstance enclosing more or less numerous lacunae, from whichradiate their minute canaliculi. It is very poor in vascular canals.The lacunas present a simple concentric arrangement; they may becomparatively few or many in number ; they may be round or ovalin shape, with few or again many canaliculi ; and the bone may showan approach to the simplest form of lamination.1The second type (pi. i, fig. 2) is composed of groups of concentriclaminae which show vascular canals running parallel to tf\e axis of thebone, as well as about the laminae, and are frequently crossed bysmaller canals running in various directions. The lacunae are con-siderable in number, and may be oval, or long and narrow, accordingto the species.The third type (pi. 1, fig. 3) is composed of Haversian systems,such a system is defined by Cunningham as follows : " The Haversiansystem consists of a central or Haversian canal which contains a vesselof the bone. Around this osseous lamellae are arranged concentri-cally, separated here and there by interspaces called lacunae, in whichthe bone corpuscles are lodged. Passing from these lacunae are manyfine channels called canaliculi. These are disposed radially to theHaversian canal and pass through the osseous lamellae. They areoccupied by the slender processes of the bone corpuscles."These three types, either singly or in combination, enter into theformation of the femora of all animals ; and there is no suggestion ofany additional form of bone structure. Taken as a whole, combina-tions of types are more common in the structure of bone than singletypes, and are more frequent in the mammals than in the classes belowthem.
1 The term lamella is restricted in this paper to the small concentric layers obone surrounding the Haversian canal, while that of lamina; is applied to thelarger more or less irregular rings of bone that run concentrically in relationto the medullary canal.
NO. 8 HISTOLOGY OF THE FEMUR FOOTE 3As to the significations of these types, the subject has been studiedfrom the following standpoints :(i) The grade of the animal in biological classification.(2) Geographical location.(3) Sex -(4) Age.(5) Function.(6) Individuality.(7) Health; and(8) Heredity.1. The first type of bone appears as the basic structure in theamphibians, reptiles, birds, and mammals. It exists, in a pure or butlittle complicated form, throughout life, in the amphibians, in the liz-ards, in some of the birds, and in the bats, excepting the Pteropus. Itexists or predominates in the fetal life of higher animals, includingman. It may well be regarded as the simplest and oldest or funda-mental form of bone structure. Its first variation is shown by a changeof the round or oval to long and narrow lacunae, by a more con-centric arrangement of the lacunae, and by increase in vascularity,which is accompanied by a change from the first to the second or thirdtype of bone structure.The second or intermediary type of bone structure develops as arule from the first type and represents often, though not invariably,a stage in the differentiation of the bone from the first to the thirdtype. Traces of it are seen first in the amphibians and reptiles, whilemore pronounced instances of it occur in a few birds, some of themammals, and at some stages of development, especially in someraces, in man. It is best represented in certain mammals, such as thevarious deer.The third. type, foreshadowed in a few amphibians, appears in partin some of the reptiles and a few birds ; it is more strongly repre-sented in certain mammals, and is characteristic of man.2. The effect of geographical position upon bone variation is notyet reducible to exact deductions. However, it is a fact that thefemora of the African and Asiatic elephants differ from each othervery materially.3. As to sex, the femora examined showed no evidence that this isan important factor in the minute structural variation of the bone.4. Age influences the type of the bone very greatly ; at least so inthe higher mammals and particularly in man. All femora of highermammals, and especially man, change in structure with advancing
4 SMITHSONIAX MISCELLANEOUS COLLECTIONS VOL. 6ldevelopment of the subject. Some femora, however, arrive at a com-pletion, or rather at a cessation of the changes, regardless of the stagereached, earlier than others. The only future change in such bonesis senility. The progress, however irregular or incomplete it may be,is always from the first towards the second or the third type, never thereverse.5. The effect of function upon variation in bone structure canscarcely be doubted, but the exact causes and effects are as yet difficultto determine. In the study of 50 genera of bats, the small Pteropuspresents still, like the rest of the bats, the first type of bone structure,while the large Pteropus shows already an early and crude thirdtype in process of formation. In a turkey of 16 pounds weight onlythe second type appeared, while in a turkey of 32 pounds weightthere was noticeable a number of Haversian systems. In manyfemora of all classes the linea aspera, the most " functional " part ofthe bone, is composed chiefly of third type units regardless of thetype of the rest of the bone. Finally, a lack of function in an adultbone doubtless favors an earlier setting in of senile changes.6. Individual variations are rare in the lower vertebrates andincrease in frequency in the higher forms. But they are mostly ofsecondary importance, the characteristic structure in species remain-in^ pretty true. The slight variations present are probably partlyaccidental, partly hereditary and partly functional.7. Variations due to health and disease remain very largely forstudies in the future. They will be almost wholly restricted to man.8. Hereditary influence finally, is clearly demonstrated by the pre-dominance of a certain form of structure in every given species. Infamilies the subject needs much further attention.DETAILS CONCERNING GENERAAMPHIBIANSThe amphibians present the following conditions
:
1. Simple first type bone with round and oval lacunae and fewcanaliculi. In some forms cancellous bone occupies the medullarycanal ; this is seen, for instance, in the Amblystoma tigrinum, one ofthe most primitive amphibians.2. A division of the simple bone into two concentric laminae,external and internal.3. A differentiation into external, central and internal laminae ; and4. In a few amphibians, as in the Toad group, very crude Haver-sian systems become outlined in the central lamina. These primitive
NO. b HISTOLOGY OF THE FEMUR—FOOTE 5
systems are composed of Haversian canals communicating' with adja-cent lacunae by a few canaliculi. No concentric arrangement of thelacunas and no Haversian system lamellae are in evidence.REPTILIANSThe reptilian femora show much the same conditions as those ofthe amphibians, but the differentiation of bone structure has in someforms advanced to a greater extent. Some species present the simplefirst type of bone. This is especially the case in the lizards. But inthe turtles, curiously, a fairly well developed third type of bonestructure has made its appearance. Again cancellous bone, which isnot a structural feature of the lizards, is generally present in .theturtles. These are remarkable differences and separate widely thetwo genera. BIRDSBirds present in general the appearance of an incompleted develop-ment of the structural state. The first, second, as well as the thirdtype of bone structure are found, and also various combinations, but allgive the impression of incompleteness. The bone units are ratherdim and unsatisfactory. The first type is present in some birds and isgenerally of a very simple form. The second type appears in a largernumber of species and is, perhaps, the most representative type inbirds. In some of these femora a few Haversian systems appear,especially in the posterior ridge, and in some birds of large size thesecond type structure is reinforced by some Haversian systems inthe anterior wall. Finally, in a few species the central ring of lamellaehas become displaced by Haversian systems and the bone must beclassified as that of the third type. As a rule the systems are ratherdim and do not stand out clear cut. Their lacunae are oval and theircanaliculi bushy. In a few birds the medullary canal is occupied bycancellous bone. In about half the bird femora the medullary canalsare full of marrow, while in the remainder they are empty. Com-paring the birds with the reptiles, there is a distinct increase in theproportion of differentiation, although this has not reached fulldevelopment. MAMMALSIn these animals the bone structure is in general much more differ-entiated than in birds. As a rule the types and their combinationshave lost the illy defined characters so frequently present in the fore-going classes. Furthermore, type combinations are more common.
6 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 6lThe first type is present in certain genera. It was found in 50different genera of bats and a number of genera of shrews. In a fewof these forms the division of the bone substance into three concentricrings has occurred. In one genus, the Pteropus, this modification iswell marked, and beyond that, rather crude Haversian systems arefound in the central ring, the bone showing thus an advance towardthe third type.Quite a large number of mammalian femora present a well markedsecond type structure. The laminae are well developed, and encloselong, narrow lacunae, with straight canaliculi. In all these bonesHaversian systems are found in the posterior ridge corresponding .tothe linea aspera. A few mammals show a pure third type of bonestructure. In such animals the first and second types are eliminatedand fully developed Haversian systems have taken their places. Butonly three or four of the 178 mammalian femora (other than bats andshrews) examined were composed of .this type.By far the greatest number of mammalian femora shows combina-tions of the first and third type. In these bones the structural unitsare well developed, but vary much in proportions. But they fre-quently occupy the same relative positions. The laminae, with bonestructure of the first type, are external and internal, while the Haver-sian systems occupy the central ring. The second and third typesform the structure of also a large number of mammals. In this com-bination the units are well developed and about equally important.Finally, in still another large group of mammals, the femora show allthe first, second and third types of bone structure, in varying pro-portions.Looking over the mammals as a whole, it is noticed that theirfemora exhibit structural differentiation much more advanced anddefinite than that observed in the femora of other animals. Fromspecies to species there are many variations.It is a peculiar fact that amphibians, reptiles, birds, and mammalsall present, though in a widely varying proportion, the first type aswell as some form of advanced type of bone structure. The advancedtype is the variable factor and occurs in the greatest variety of formsand combinations. The early or first type differs merely in simplicity.It is more simple in the amphibians than in the mammals. The thirdtype, on the other hand, in amphibians, merely a suggestion, is betterdeveloped in reptiles, still better in birds and in mammals reaches itshighest state of advancement. Clean cut, well developed third type
NO. 8 HISTOLOGY OF THE FEMUR—FOOTE J
units are not at all common below mammals, but are the importantstructures of mammals and especially man.MANThe human fetus presents in varying combination the first andsecond type of structure with wide canals and incompletely formedlacunae. As development progresses, the first and second type boneis gradually displaced by the Haversian system structure.More in detail, in the very young human fetus of two to threemonths, the first type of bone structure is present in an incompleteform and is marked off into irregular areas by crude, branchingcanals. As fetal life advances the canals become less branching andmore concentric. Gradually the first becomes the second type ofbone and remains so until about one year after birth, when sufficientdifferentiation has occurred by the formations of Haversian systemsto make it second and third type, or first, second and third type com-bination. Throughout childhood and youth, the laminae tend to dis-appear and to be replaced by Haversian systems, until the bone devel-opment is completed. In the early period, a horseshoe-shaped bandof laminae is often observed forming the anterior and lateral walls ofthe bone. A remnant of this horseshoe may remain throughout lifein those femora which do not complete the third type differentiation.The proportion of this remnant to the other bone units in the adultbone varies greatly and the result is that adult femora present manysecondary variations.A white child, a Pueblo Indian, and a Peruvian Indian child, eachabout one year of age, exhibited already a combination of the secondand third types of bone structure. A femur of an Egyptian child ofthe Xllth Dynasty showed the development of the Haversian systemdirectly from the circulation, which is an evidence of the causal asso-ciation of bone structure with the development of the vascular systemof the bone.On the whole, the study of human femora from fetal life and child-hood shows various transitional stages from the first and second to thethird type of bone. ADULT HUMAN FEMORAThe adult human femora are, in general, characterized by the pre-dominance of a well differentiated third type of structure. An
8 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 6l
exclusive presence of the first type of structure has never been foundin the adult human femur. The most primitive form is a combina-tion of the first and third types. The proportions of the structuralunits varies greatly. In some femora, the first type was found toamount to more than half of the section, while in others it is reducedto a small fraction. In other human femora there will be a second andthird, instead of first and third type combination ; and still others, thebone shows all the three types. When the first type is present, it isgenerally found in the form of a horseshoe band extending under theexternal surface of the bone—the heel of the shoe embracing theposterior ridge. Segments of laminae with a first type of bone, fre-quently found in bone sections, are the remains of a disappearinghorseshoe band of first type units. In a complete third type bone, thefirst and second type units have been entirely displaced by welldeveloped Haversian systems. There may be cancellous bone aroundthe medullary canal.Three human races have been examined, namely, the black, thewhite (including the ancient Egyptian), and the yellow-brown. Anearly and late differentiation has been found in each. The negro,modern white, Egyptian of the Xllth Dynasty, the Pueblo andPeruvian Indians all show these variations. The variations are thesame in kind, but somewhat different in degree. The negro bone,barring individual exceptions, does not perhaps equal that of theother races in the degree of the differentiation.The posterior ridge is generally composed of Haversian systems.This occurs in each race.Senile changes, absent or very rare in animals, are unexpectedlyfrequent in human femora, particularly those of civilized races.SENILE CHANGESAfter a human bone has reached its developmental limitation andperhaps the climax of its function, it soon begins to undergo certainchanges which are properly those of degeneration of senility. Suchchanges are evidently far more common than is supposed. Age inyears is not to be the determining factor. A femur may be more orless senile at 30 or 40 years of age. There is no structural differentia-tion beyond the Haversian system type; when that has been com-pleted it may remain as such for years, but sooner or later a processof aging sets in. The senile changes begin around the canals of theHaversian systems. They involve first the systems around the medul
NO. 8 HISTOLOGY OF THE FEMUR—FOOTE
lary canal. As the changes extend the bone becomes lighter inweight and its walls become thinner (pi. 3, figs. 1, 2, 3, 4, 5). It isa slow destruction.TABLE OF TYPE PERCENTAGES
NumberFirst typeSecond typeThird typeFirst and second type.Second and third typeFirst and third type. .First, second and thirdtypeUndeveloped thirdtypeMedullary canal, full.Medullary canal,emptySenile
Amphibians
3497%0.3%
3%100%
Reptiles

SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 61, NO. 8. PL. 1
#*H
Fig. 1
fl&
Fig. 3THE THREE TYPES OF BONE STRUCTUREFig. i.—First type as seen in the amphibian, Nyctalus aviator.Fig. 2.—Second type as seen in the turkey.Fig. 3.—Third type as seen in n?an.

SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 61, NO. 8, PL. 2
Fig. 1 Fig. 2
Fi 9- 3 Fig. 4SECTIONS OF FEMORA, SHOWING VARIOUS COMBINATIONS OF TYPES.
vlr' l'~f^K femur °J a sIoth bear - Melursus labiatus. No. 2272, A. M. N. HF r' ,' p '?ur of a Jackal, canis. No. 7172, U. S. N. M.T?,°' 3-—KTght femur of a coyote, canis latrans.ig. 4.—Left femur of a badger, taxidea Americana.

SMITHSONIAN MISCELLANEOUS COLLECTION VOL. 61 NO. 8, PL. 3
Fig. 1
Fig. 2 Fig. 3
Fig. 4 Fig. 5SENILE CHANGES IN THE HUMAN FEMURFig. i.Fig. 2.Fig. 3.Fig. 4.-Fig. 5. i;
esin fJ^H=, l a .«>lore? man - Large black spaces represent senile absorption of bone.-A g e Haversian system, much enlarged, without definite signs of senility.A sin?if Savers .,an system, muc ,h enlarged, showing early signs of senility.- gle Haversian system, much enlarged, showing a later stage of senility.
-A single Haversian system, much enlarged, showing the latest stage of senilitv.