Functions of the Haversian System

DONALD H. ENLOW Department of Anatomy, The University of Michigan, Ann Arbor, Michigan

The Haversian system or osteone has associated with areas of re-location in mus- been traditionally adopted as a universal cle attachment on a growing , and in unit of structure in compact bone. The remodeling processes involving resorption basic functions and the structural signifi- of periosteal bone surfaces during nieta- cance of primary and secondary Haversian physeal reduction in diameter axd re- tissue, however, are poorly understood. gional changes in shape. The hypothesis Two explanations on the functional mean- is advanced that this type of Haversian ing of the secondary Haversian system system functions as an anchoring mecha- have been proposed. These are (a) the nism which can maintain muscle con- interpretation of the osteone as an ex- tinuity and attachment with bone during clusive response to stress, and (b) the such remodeling changes. All secondary interpretation of the secondary osteone as osteones, regardless of particular function, an exclusive structural result of mineral are structurally comparable and represent mobilization and redistribution. However, a product of internal reconstruction with- the characteristic absence of the Haver- in compact bone. sian system in the compact bone of many History. Leeuwenhoek (1678) was the vertebrate species, including widely used first to notice the microscopic canal sgs- experimental forms such as the white rat, tern in bone, and he reported his observa- and the characteristic patterns of distribu- tions to members of the Royal Society in tion of Haversian systems in the bone of a series of personal communications which those species which do possess these were later published. Soon after, Clopton structural systems, cannot be entirely ex- Havers presented several lectures before plained on the basis of these existing func- the Royal Society in which he described in tional concepts. This report will propose greater detail the microscopic structure of that the Haversian system has several bone and joints. Havers, a versatile basic, previously unrecognized functions. English physician, later compiled his ex- The bone tissues from a large number of tensive observations and published the individuals and from a variety of species first monograph, “Osteologia Nova,” deal- were studied in an attempt to establish the ing with the structure and function of developmental, functional, and structural bone as a tissue (1691). Havers did not relationships which are associated with recognize or first identify the Haversian the process of secondary Haversian recon- system, but he did describe in some detail struction. It was found that localized or the “longitudinal and transverse pores” in widespread areas of lion-pathological compact bone. These were becoming gen- necrosis can be present as a erally known, by the middle of the eight- natural condition in specific types of bony eenth century, as the canals of Havers tissue, and that resorptive and reconstruc- (Albinus, 1757). Havers suggested that tive activity may be associated with such canals in compact bone function to trans- regions. It is suggested that the secondary port medullary oils in order to “mollify” osteone can function as a replacement the substance of the bone, and he believed mechanism in the internal reconstruction that the canals located near the ends of and reorganization of in cor- the bone carry lubricating oils to nearby tical areas involving necrosis. joints. These logical notions were popu- A variety of the secondary osteone, in- larly accepted and persisted for another dependent of necrosis, is characteristically half a century (Monro, 1763). It is in-

269 273 DONALD H. ENLOW teresting to remember that one entire findings. It will be demonstrated that school of thought, led by prominent anat- areas of bone necrosis appear in definite omists and physiologists as late as the patterns of distribution and with predict- nineteenth century, denied the existence able structural relationships. of any canal system in bone (Bostock, 1825). Several early writers observed MATERIALS AND METHODS blood vessels in the larger spaces of Formts studied. Bone tissues from 89 bone, but Albinus (1757) confirmed Rhesus monkeys, from 29 dogs, and from the presence of vessels in small cor- survey samples of other representative tical canals by the use of vascular in- vertebrate groups were examined for (a) jection methods. The Haversian system of the distribution and structural relation- concentric lamellae with its central canal ships of primary and secondary Haversian was described, defined, and named by tissues, and (b) the presence and distribu- Todd and Bowmann (1845). The Haver- tion of non-pathological necrosis in com- sian space (resorption canal) was identi- pact bone. In order to determine the se- fied by Tomes and DeMorgan ( 1853), and quence of Haversian changes and age re- these workers were the fbst to recognize lationships, observational data of monkey that the Haversian system represents a bone tissues were organized according to substitution mechanism. The term “oste- primary, mixed or permanent dentition. one” was introduced by Biedermann (’14), Bone from the femur, tibia, humerus, and the hypothesis that the osteone de- radius, and mandible was studied in most velops as a mechanical response to ten- of the monkeys. Multiple, entire trans- sion was formulated largely by Gebhardt verse sections were made through many of (’05). Biochemical considerations rela- the from their proximal to distal tive to the interpretation of secondary bone ends. reconstruction have been investigated and Experimental necrosis. To test the re- discussed by Amprino (’48, ’51, ’52) and sponse of secondary Haversian reconstruc- by Ruth (’53). The presence of secondary tion to the presence of necrotic bone, lo- osteones near a periosteal surface, par- calized areas of diaphyseal bone in the ticularly in bony tuberosities, was noticed femora of white rats were experimentally by Petersen (’30), and he termed these necrotized. The bone was exposed by Haversian systems “marginal osteones” surgical entrance through the lateral in- (Randosteonen). termuscular septum. The was It is well known that necrotic bone tis- reflected, and an area measuring about sue can be associated with a variety of 2 mmz was necrotized by thermal cautery. pathological processes, particularly those The animals were sacrificed at intervals involving vascular interniption. Empty through a period of 6 months. The cauter- lacunae in areas of dead bone were ob- ized areas were then examined histolog- served by Barth (1895). Necrotic bone, ically and compared with normal bone in unrelated to pathological processes and the opposite femur and with bone from located specifically in interstitial areas control animals. (between Haversian systems), was noticed Methods of tissue preparation. Ground by Mueller (’26), J&e and Pomeranz thin-sections were made using a power- (’34), by Sherman and Selakovich (’57), driven polishing lap wheel. To demon- and by Frost (’60). These workers did not strate canalicular calcification in necrotic suggest that the Haversian system func- bone (a process to be considered later), the tions as a specific replacement mechanism thin-sections were coated with an impervi- in response to the presence of necrosis. ous seal of parlodion (Enlow, ’54), or were By counting proportions of empty lacunae impregnated with fuchsin or silver nitrate in random microscopic fields, Frost con- (Frost, ’60). Using these techniques, firmed the proposition that necrotic bone areas in which canaliculi have been filled in the human is more frequent in older with mineral (“micropetrosis”) appear individuals, and that it is more widespread transparent and are easily recognized. jn extra-Haversian bone. The results of The transparent nature of this bone is the present study are consistent with these due to the absence of trapped air normally FUNCTIONS OF THE HAVERSIAN SYSTEM 271 present in canaliculi as viewed in ground The presence, distribution, and extent of sections. Ordinary mounting of ground normal osteocyte necrosis appears to be thin-sections in balsam or other standard directly related to the particular arrange- media without such treatment will give ment of tissue components involved in the uncertain results, since seepage of the structure of that bone. Areas of bone media into unprotected canaliculi may which are composed predominantly of displace the air and thereby prevent dif- primary osteones or of a closely-meshed, ferentiation between areas of micropetrosis symmetrical network of primary canals and areas in which the canaliculi are not (“Plexiform” bone, fig. 11; Enlow and filled with mineral. Micropetrosis cannot Brown,’ 56) seem to be relatively resistant be recognized in decalcifred preparations. to the appearance of necrosis, since re- Microradiographs were compared with gions of empty lacunae are infrequently ground sections in order to determine pos- observed. The distribution of canals in sible differences in radio-density between these tissues is typically dense. Ordinary vital bone and necrotic areas containing circumferential lamellar bone which coii- canalicular calcification. tains a crowded concentraiion of primary Decalcified and stained sections were vascular (non-Haversian) canals also ap- prepared by standard methods using a pears resistant to necrosis (fig. 3). The microtome. Preparations were also made degeneration and subsequent disappear- by a special technique in which ground ance of seems to occur initially thin-sections were decalcified and stained at selective focal points which are farthest (Enlow, ’61a). This method gave assur- removed from adjacent vascular canals ance that necrotic areas were not regions (fig. 1). In a microscopic section of any of artifact resulting from poor fixation. bone, the pattern of necrosis depends Early in the study, sections were prepared largely on the amount and pattern of any from tissue blocks 2-5 mm thick, but sparsely vascularized, circumferential la- there was still concern that empty lacunae mellar bone which is present in that sec- (an indicator of necrosis) might be a re- tion. Necrotic bone may appear, thus, as sult of incomplete fixation. To exclude isolated patches (figs. 1, lo), or in a wide- this possibility, blocks of bone were re- spread circumferential zone (fig. 2). As moved from animals immediately follow- an area of necrosis becomes enlarged iii ing sacrifice, and polished thin-sections extent, cells in those regions immediately approximately 80-1 10 II were prepared surrounding canals may also die (fig. 6). and decalcified at once in Decal solution.’ In extreme or advanced necrosis, primary They were washed and then placed in osteones and plexiform bone can become 10% formalin. A paper-thin, completely involved, although this situation has not decalcified section of bone, therefore, was often been observed. exposed to the fixative in not more than Examination of a variety of skeletal ele- 30 minutes following death. Sections in ments from the same individual, and of this range of thickness contain 4 or 5 multiple sections made at different levels layers of osteocytes, thereby insuring com- from the same bone, indicates that the plete enclosure and protection of cells. distribution of cellular necrosis is deter- Microtome preparations were sectioned at mined by the particular combinations of about 50 II, since very thin sections will tissue types present, as described above. In not demonstrate all nuclei present. view of the consistent and predictable fre- Cellular necrosis in bone. Areas of quency in the occurrence of necrotic tis- bone which involve osteocyte necrosis may sue, the presence of limited ostemyte be identified, in decalcified and stained necrosis is considered a normal or natural sections, by the absence of nuclei within situation (table 1). lacunae. Using routine methods of prep- Based on these observations, it may be aration, intercellular tissues appear other- stated that, in general, a greater density i:i wise unchanged. In any local or extensive the number of vascular canals in any re- region of necrosis, most or all of the lacu- gion of compact bone favors a greater re- nae within that region are totally devoid sistance in that particular bone locality of cells. 1 Scientific Products, Evanston, Illinois. 272 DONALD H. ENLOW to the death of its osteocytes. Conversely, necrotic bone and with all surrounding a sparse distribution or total regional ab- lacunae lacking cells, demonstrate an in- sence of vascular canals is conducive to creased number and distribution of re- local cellular degeneration and necrosis. sorption spaces and formative secondary Death in any population of osteocytes is osteones (table 2, figs. 4, 5, 6, 7). It is a regional situation which is governed by significant to note that such secondary the pattern and arrangement of component Haversian formation can be located in re- tissue types. gional zones of compact bone which, in Resorption spaces. Bone tissues in individuals of the same species possessing which canals are partially or completely only living bone, characteristically lack surrounded by a community of living secondary osteones. The resorption spaces osteocytes but which contain scattered, represent enlarged cavities derived from isolated patches of necrotic bone in in- canals located immediately within the re- terstitial areas between canals, have been gion of necrosis. The fact that necrotic obsen-ed to demonstrate infrequent, scat- areas can occur prior to resorptive activ- tered resorption spaces. However, bone tis- ity (fig. 1) suggests that Haversian re- sues containing areas of extensive necrosis placement is not necessarily an immediate in which cands are located directly within process and that a period of time is in-

TABLE 1 -~ Rhesus monkeys Dogs Primary Mixed Permanent Unknown ,,%:- dentition dentition dentition dentition .~ __ Absent 17 18 13 13 23 Scattered patches 4' 2 2 4 2 Microsetrcsis' (as in fig. 15) Extensive 0 4 7 0 2 (as in fig. 16) Absent 5 3 0 7 5 Scattered patches 0 3 15 9 20 Necrcsis (as in fig. 10) Ex teiisive 0 0 3 4 (39 in fig. 2)

1 Specimens examined for micropetrosis were not necessarily checked for osteocyte necrosis, since some bone samples were available only in a dried condition. The total number of specimens for which micropetrosis is reported, therefore, is larger than the number examined for cellular necrosis. Dried specimens. Extent of osteocyte death not known.

TABLE 2

,",","ls~~s Dogs Resorption spaces Resorption spaces number of number of in necrotic bone1 in living bonel.2 Necrosis individuals individuals examined examined monkeys dogs monkeys dogs

Absent 15 5 0 0 24 26 Scattered patches 27 20 31 14 92 118 (fig. 10) Extensive 4 4 95 215 8 26 (fig. 2)

~~ 1 Total number of resorption spaces and partially-formed secondary osteones from transverse, mid- diaphyseal sections of the femur in all specimens. Resorption spaces and formative osteones in areas of muscle attachment and in areas produced during endosteal growth are not included re- gardless of necrosis present, since such secondary reconstruction may result from other growth circumstances. 2 Characteristically located in periosteal bone on or near a reversal junction between endosteal and periosteal zones of the cortex. FUNCTIONS OF THE HAVERSIAN SYSTEM 273 volved. This is supported by the expen- ones. The secondary osteone, thus, ap- mental findings to be described in a later pears to be a structural product following section and by the data presented in table the superimposition of a newly formed 2. Whether or not “buds” from nearby population of living bone cells within older canals in living bone can penetrate and re- regions of localized dead bone. Remnants place adjacent necrotic bone has not been of former necrotic bone which are not determined. Observations of blind canals completely replaced now persist as dead (Dempster and Enlow, ’,59)suggest this interstitial bone tissue between Haversian possibility, but it may also be true that systems (figs. 6, 7). such canals represent plugged osteones Currey (’60), in comparing the blood (Cohen and Harris, ’58). Closed canals supply of Haversian and plexiform bone, have been observed in microscopic sec- comments that Haversian bone is less tions, particularly in areas of extensive “efficient” than the latter. This conclu- necrosis. Lacunae surrounding such sion is consistent with the observations canals are typically empty. reported in the present study. Currey specu- Age relationships. The conspicuous ab- lates that the presence of previously estab- sence of major necrotic areas in younger lished Haversian systems may cause the individuals (table 1) can be attributed to eventual death of surrounding interstitial the almost exclusive presence of richly cells and that this would be followed by vascularized bone. Compact bone in such an increase in the number of secondary forms is composed of either closely packed osteones produced during progressive re- primary osteones, plexiform bone, or of placement. It has been assumed by earlier lamellated bone tissue containing a dense workers that the relative immunity of the concentration of simple, primary vascular Haversian system to necrosis, compared canals. As described earlier, these bone with interstitial bone, is attributable to types are less sensitive to necrosis than the isolation of interstitial tissue from its thick expanses of lamellar bone containing vascular supply (Mueller, ’26; Jaffe and only scattered vascular canals. With in- Pomeranz, ’34; Frost, ’60). That the proxi- creased age, and as local growth rates and mity of the vascular supply is a significant remodeling alterations result in progres- factor in the presence of necrosis has been sively changing tissue combinations, in- discussed, and this situation is true also creased deposits of sparsely vascularized, for the Haversian system. However, the circumferential lamellar bone accumu- characteristic, selective localization of re- lates. This latter variety of bone, found in sorption canals and secondary osteones quantity only in individuals beyond very within necrotic bone, which was previously young age, is the tissue type most com- primary in nature, strongly supports the monly associated with necrosis. During replacement interpretation of this second- periods of active skeletal growth, new cell ary tissue. populations are constantly being added With the continued reappearance of and older cell communities are being re- necrosis, secondary osteones themselves moved as bones change in size and re- may succumb to osteocyte death. These gional shape. When adult proportions are are then partially replaced by newer sys- reached, this process becomes slowed so tems (fig. 17), and second and third gen- that subsequent changes within compact erations of superimposed Haversian sys- bone proceed largely by jntemal Haver- tems are thereby produced. sian replacement. Species correlation. Growth rate in Placement of secondary osteones. Con- conjunction with animal size and longev- forming with the distributional pattern ity determines the particular combinations observed in the arrangement of resorption of basic bone tissue types found in the canals, secondary Haversian systems are skeleton of any vertebrate species. Exam- selectively positioned in either regional or ination of bone tissues from a variety o€ extensive areas of necrotic bone (figs. 4, representative vertebrates indicates that 5, 6, 7). Deposition of concentric lamel- species having bone tissues composed lae within resorption canals will convert largely of tissue types which are more these spaces directly into secondary oste- resistant to necrosis, as described above, 274 DONALD H. ENLOW do not possess significant amounts of true which determine why they do or do not secondary Haversian tissue in periosteal develop, since the rat normally does layers of the cortex. Examples would in- not possess secondary Haversian systems clude most amphibians, some reptiles, and whereas certain other species do. To say a great many smaller mammals, such as that the functional significance of the the white rat. Conversely, species which Haversian system is a singular result of characteristically have more massive de- calcium need and mobilization followed by posits of circumferential lamellar bone redeposition would be overextending the containing a relative deficiency of vascu- conclusions of Ruth’s study, which the lar canals, as in portions of the human author did not intend since his purpose skeleton, commonly possess more or less was to demonstrate the osteone as a mech- extensive areas of secondary Haversian anism of replacement. Similarly, the par- bone. Even in older human bone, how- allel response to cautery-induced necrosis ever, much primary although densely demonstrates a laboratory circumstance vascular bone can be found. Secondary which can produce secondary reconstruc- Haversian tissue, in any species typically tion. In itself, this does not confirm that exhibiting this particular bone type, can the Haversian system is a unique result of be arranged in isolated clusters or as ex- regeneration following necrosis. It does, tended zones depending on the pattern and however, indicate that the observations extent of necrosis. described in this study can be reproduced Experimental evidence. To test ex- experimentally. perimentally the response of secondary Canalicular calcification. In associa- Haversian reconstruction to the presence tion with natural necrosis, a normal condi- of aseptic necrosis in a species which does tion can be present which involves the not normally have either widespread bone deposition of mineral within canaliculi. necrosis or secondary Haversian systems, Soon after the surprisingly recent dis- small areas of cortical bone in the white covery of lacunae by Deutsch and Purkinje rat were necrotized by thermal cautery. in 1834 (Leeuwenhoek may have seen An encrusting callus developed around them in the late 1600’s but his descrip the periphery of the necrotic area and tions are vague), there was much specu- eventually covered it. The initial stage of lation concerning their contents. It was the callus involved the formation of fine suggested by Muller (1834) and Miescher cancellous, non-lamellar bone with sub- (1836) that the lacunae with their canal- sequent lamellar compaction. Immediate, iculi are filled with chalk (“sacculi and extensive resorption and replacement of canaliculi chalicophori”). Eruns (1841) necrotic bone did not take place. Within and Gerlach (1848), using injection tech- the six-month period, typical scattered re- niques, demonstrated that they are hollow sorption canals had appeared within areas in ground sections and suggested that they of necrosis, and concentric lamellar de- contained plasma in living bone. Lessing position within these spaces was observed (1846) showed that lacunae and canal- (fig. 26). This is the same formative iculi appear dark in dried thin-sections sequence involved in secondary Haver- due to the presence of air, and he argued sian formation. that they represent an air-filled lacunar The results of this experiment must be system in life. But during the same perid, interpreted in perspective. The experi- the cell doctrine was becoming establishex. ment performed by Ruth (’53) demon- The presence of nuclei and cytoplasm in strated that secondary osteones can de- the lacunae of was identified by velop in the rat by artifically induced, Schwann (1837), and cells located in the severe calcium deprivation (causing re- lacunae of bone were reported by Mayer sorption) followed by a period of dietary (1841) and by Donders (1848). Tomes calcium excess (available calcium for re- (1843) confirmed the cellular nature of generative redeposition). This work dem- bone tissue, but he also recognized and onstrates how secondary osteones can de- reported that many canaliculi can be velop under controlled conditions. It does filled with mineral. This observation was not, however, define natural circumstances recently rediscovered by Frost (’60), who FUNCTIONS OF THE HAVERSIAN SYSTEM 275

correctly related canalicular calcification individual, (c) in different ages of the with osteocyte death. He has termed this same species, and (d) between different process “micropetrosis.” Calcified canal- species. The formation of the true second- iculi appear to be comparable with scle- ary osteone, which is concerned with the rotic or transparent dentin (Orban, ’57), internal reconstruction of compact bone, in which dentinal tubules within dead can also be involved in general remodeling tracts are plugged with mineral deposits. processes concerned with the gross shap- Patterns of distribution and structural ing of bone during growth. The develop- relationships. Areas of micropetrosis can ment of this particular variety of the appear (a) in interstitial bone (figs. 17, Haversian system may be quite independ- 24), (b) as isolated patches (fig. 15), or ent of necrosis. (c) as extensive circumferential zones or Secondary Haversian formation regu- layers (figs. 16, 18). Micropetrosis, when larly occurs in defined areas, so that dis- present, may often be recognized macros- tinct “Haversian zones” can be identified. copically on cut surfaces of bone by its The shifting of zones following gross re- transparent appearance. The initial on- modeling changes will often result in the set of micropetrosis appears in restricted relocation of such Haversian zones into spots located within thick lamellar bone new positions within the cortex. Haver- containing relatively few vascular canals. sian bone associated with muscle re-at- Calcification near canals seems to be tachment, for example, and with endosteal avoided until the extent of the micro- growth or with cancellous compaction, petrosis becomes more widespread (fig. can come to lie deep within the cortex in 16). Microradiographs of micropetrotic a new relationship at some distance from bone (figs. 20, 21) show that the overall its former location. density of the matrix, when compared with Bone structure in areas of muscle at- adjacent areas of vital bone, is not notice- tachment. The composition and arrange- ably affected in the bone of the young, ment of bone tissue within prominent proc- growing individuals examined. esses, depressions, or unmodified bone Both resorption spaces and secondary surfaces to which muscles or tendons at- osteones are frequently and characteris- tach can be distinctive. Within such re- tically located in areas of micropetrosis gions, concentrations of secondary oste- (figs. 15, 18, 19, 24). Interstitial micro- ones are observed as a characteristic and petrotic bone between secondary osteones localized component (figs. 8, 23). The represents the remnants of older necrotic initial formation of these secondary sys- tissue (fig. 17). tems is not a response to necrosis, although It is apparent that the distribution of this process can also be involved as inde- canalicular calcification coincides both in pendent complication (fig. 12). pattern and structural relationships with During longitudinal growth of a bone, necrosis. Necrosis, sometimes even rather muscle attachment necessarily becomes widespread in extent, can be present in a shifted as a muscle is relocated in its mi- bone, yet that same bone may or may not gration up or down the elongating shaft. show micropetrosis. Apparently, calcifi- Also, the sectional shape of a bone under- cation of canaliculi is a sequel to necrosis. goes considerable change during meta- Relationship of secondary reconstruc- physeal-diaphyseal transition. If tuber- tion with gross remodeling. The progres- cles are involved, a continual “drift” in sive remodeling of a bone during its the relative location of the tubercle takes postnatal growth involves considerable re- place during remodeling. Continuous re- organization and alteration in the minute lease of muscle insertion is required in structure of the bone tissue itself (Enlow, this process, and progressive muscle re- ’61b). Detailed analysis of this remodeling attachment must be maintained during process makes possible a developmental such growth changes. There is no prob- interpretation of the complex architectural lem if the shift in location involves simply patterns and structural combinations ob- periosteal deposition of new bone enclos- served (a) in different areas of the same ing new Sharpey’s fibers. But if muscle bone, (b) in different bones of the same attachment is to be preserved on a sur- 276 DONALD H. ENLOW face undergoing active resorption rather endosteal growth in combination with cor- than deposition, the continued insertion responding periosteal resorption. Spongy of that muscle must survive even though bone in the medulla of the is the bone into which the muscle is attached converted into compact, cortical bone as is being removed. If rate of growth is the metaphysis is relocated in position to relatively slow, this is apparently accom- become the . Considerable re- plished by waves of localized resorption modeling and internal reconstruction can and surface apposition, so that at least be involved. The original trabeculae of parts of a muscle are anchored at any one fine-cancellous endochondral bone are time. The process involved has been dis- partially removed and replaced by lamel- cussed by Petersen (’30). In species lar trabeculae of coarse-cancellous bone. which show periods of rapid skeletal This coarse-cancellous bone itself is sub- growth, however, the structural arrange- ject to extensive removal, replacement, ment illustrated in figure 13 is common. and structural readjustment. Reversals in The tubercle is drifting across the surface direction as the bone grows outward, in- of the bone. One side of this bony process ward, and then outward, together with the has received lamellar apposition whereas formation and reformation of trabeculae the opposite side is a resorptive surface. and the closure, reopening, and reclosure Muscle attachment must be maintained of cancellous spaces during these growth on a resorptive as well as on the de- reversals, produce complex patterns of positional surface. While periosteal attach- microscopic architecture. When individual ment is not necessarily completely severed trabeculae are incorporated into the cortex during periods of periosteal resorption, by compaction during inward growth, the the muscle nevertheless must be re- resulting compact bone often has a brec- located and re-attached on this resorp- ciated structure with unorganized, abrupt tive surface. The resorptive enlarge- angles of lamellar orientation. Incomplete ment of canals in the underlying com- segments or vestiges of lamellae are em- pacts and subsequent deposition of new bedded within the former trabeculae, and bone within these canals can serve to re- spaces of widely varying sizes showing establish intimate periosteal bond with progressive stages of compaction are the substance of the bone, even though present (figs, 14, 25). Structural results the surface of that same area is being produced by this process of cancellous progressively destroyed. The whole sub- compaction are associated only with endos- stance of the osteone is in direct contact teal growth, as coarse-cancellous bone is with the periosteum since the fibrous not involved in periosteal appositicn. The matrix of the entire Haversian cylinder is structure is a mosiac of osteones, demon- continuous with the fibrous component of strating a variety of irregular shapes, the periosteum. In figure 13, the second- proportions, and sizes. This characteristic ary osteones follow in the direction of type of bone can usually be recognized by the drift but are in advance of the resorp- these features, in addition to the con- tive surface. In this situation, the second- voluted, whorled configuration always ary Haversian system appears to represent present in the interstitial bone (fig. 14). a pinning or pegging mechanism which The canal system, following compaction, can serve to anchor the muscle to that may be classed as “Haversian” since each area of bone which is itself undergoing re- canal is surrounded by a concentric, often moval, or within which the attachment of irregular, lamellar sheath. Since recon- a muscle is shifting in location. A com- struction is involved to a greater or lesser parable process will be discussed below degree in the formation of this bone type, in connection with endosteal bone growth it is to be considered as secondary in na- during metaphyseal remodeling. ture. Regeneration of necrotic bone is not Compaction of coarse cancellous bone. involved in its original formation, but like Reduction in diameter of the bone during other bone tissues, it is also subject to metaphyseal and diaphyseal remodeling this process. Endosteal Haversian bone involves the lamellar compaction of coarse- resulting from coarse cancellous compac- cancellous bone. This is a process of tion is frequently found in routine section FUNCTIONS OF THE HAVERSIAN SYSTEM 277

preparations. It is typically a significant ‘‘zone” of older endosteal bone containing structural component in the compact bone secondary osteones. Remnants of such of larger species having a thick cortex. zones following extended increase in diam- When persisting in the middle third of a eter are seen in figures 15 and 16 on the , it occurs in well marked zones inner margin of the cortex. Secondary which are usually endosed on one or both osteones are commonly observed to over- sides by more recently formed periosteal lap reversal lines separating broad zones and endosteal layers. produced by inward and outward growth. The problem of muscle attachment Haversian systems located within both during metaphyseal remodeling. It is ap- periosteal and endosteal bone near such parent that the resorption of an external a junction are continuous, thereby provid- surface complicates the process of re-at- ing continuity between these two zones tachment during endosteal growth periods (table 2). involving muscle relocation. This situation Reduction in metaphyseal diameter in- is similar to that previously discussed rela- volving compaction of coarse-cancellous tive to shifts in location of muscle attach- bone will produce interstitial bone which ment and to tubercle drift in the elongating is characteristically whorled and convo- shaft. In figure 27, metaphyseal diameter luted, as previously described. Even when is being reduced by external resorption in this bone becomes relocated from its orig- combination with endosteal apposition. inal position to become a zone embedded Resorption spaces have formed in front in the cortex which is located farther down of the inwardly advancing external sur- the shaft, it can be identified and its de- face, and lamellar deposition within these velopmental relationships can be recog- spaces has proceeded proqressively in an nized. If inward growth takes place in endosteal direction. Note also that the areas of the metaphysis located near the “secondary” canals become abruptly “pri- diaphysis, however, cancellous compac- mary” toward the inner part of the cortex. tion may not be involved. In this situa- This process appears to be a mechanism tion, endosteal apposition is in the form providing progressive periosteal anchorage of extended sheets of inner circumfer- or continuity within the substance of the ential lamellae, and following Haversian compact bone. The entire cylinder wall of reconstruction during inward growth, each Haversian system is directly continu- these more regularly arranged lamellae ous with the fibrous matrix of the perios- become interstitial in position. The teum. The interstitial bone, thus, is “whorled” appearance, therefore, is not endosteal, but the network of osteones characteristic, and recognition of this embedded in this endosteal bone is perios- bone as endosteal in nature is somewhat teal in nature. Progressive lamellar de- more difficult than in other locations position in each osteone, and the subse- which involved cancellous compaction. quent formation and reformation of new That it is endosteal, however, can be con- osteones, serves to provide continua1 perios- firmed by tracing serial sections which teal attachment as the periosteal surface demonstrate the direct continuity between itself is being removed. Following rever- these two varieties of secondary Haver- sals in direction of growth, this accumula- sian bone tissue produced as a result of tion of osteones will remain in the cortex inward growth. as defined zones enclosed by other layers The classical pattern of bone structure, composed of different tissue types. The involving outer and inner circumferential bone illustrated in figure 28 is entirely lamellar layers enclosing a middle Haver- endosteal. Note the inner circumferential sian zone, can be one result of this re- lamellae, the inward-advancing secondary modeling sequence. In figure 22 the inner periosteal osteones, and the external re- layer of circumferential lamellae and the sorptive surface. The section illustrated middle zone of secondary Haversian bone in figure 29 demonstrates the relationships were both produced during inward growth. of such bone following outward reversal Following reversal, the outer layer of cir- in direction of growth. Outer circumfer- cumferential lamellae was added. It is to ential lamellae now enclose a distinct be emphasized that the occurrence of 2 78 DONALD H. ENLOW periosteal resorption in combination with cluding the dog (fig. 11). It is com- endosteal deposition is widespread during parable with the primary osteone in that the remodeling of the proximil and distal it develops by lamellar filling in fine thirds of the bone. The resulting arrange- cancellous spaces which were formed ment of structure may persist in the cortex within variable amounts of non-lamellar as these areas later become relocated into bone. Rather than forming anastomosing, the middle regions of the shaft, as in elongated osteones, however, the canals figure 22, following increase in the over- are arranged as a closely meshed, sym- all length of the bone. The consistent and metrical plexus. Like the pirmary osteone, predictable relationship of the secondary it is observed to develop in areas of osteone with this particular remodeling rapidly forming bone, and when present, process, as well as with its specific pres- it is usually distributed in widespread ence in areas of muscle relocation, sup areas of the cortex. Plexiform bone is ports the interpretation of the secondary commonly associated with periosteal ap- Haversian system as a functional mecha- position, but this type of bone has also nism providing progressive muscle anchor- been observed within deposits produced age during remodeling changes. during endosteal growth. The secondary osteone. Unlike most DISCUSSION tissues, bone contains cells which are The primary osteone. This variety of entombed in isolated lacunae within a the Haversian system (fig. 9) is formed calcified matrix. Adjacent lacunae are in- by the deposition of concentric lamellae terconnected only by canaliculi, and vas- within tubular, anastomosing spaces lo- cular supply can be far removed from cells. cated in surface deposits of fine-cancel- It has long been known that osteocytes do lous, non-lamellar bone. Secondary resorp not undergo mitotic cell division (v. Ebner, tion and reconstruction of pre-existing 1875; Broesike, 1882). The repopulation bone is not involved. Although similar in of any local area in bone with a new gen- structural appearance, primary and sec- eration of osteocytes, as in the regenera- ondary osteones represent different func- tion of necrotic bone tissue, cannot stem tional systems within compact bone. The from the mitotic division of adjacent cells primary osteone appears to be associated already present. Rather, regeneration can with either regional or widespread areas only proceed by (1) removal of bone involved in the relatively rapid accumula- through the formation of resorption tion of bone. The extent of its presence canals, and (2) reformation of young seems to be determined by the body size bone by lamellar deposition within these of the individual and rate of skeletal erosion canals. The structural result is a growth. The primary osteone is quite com- secondary osteone composed of concentric mon, for example, in the skeIeton of the Haversian lamellae enclosing a central young, growing dog and monkey, but al- Haversian canal. though present, it is relatively limited in The true secondary osteone has a re- the white rat. Primary osteones are ar- stricted but predictable distribution in (a) ranged into distinct zones which have be- the variety of vertebrate species which come enclosed by additional zones of dif- have this special type of bone, and (b) ferent bone tissue types. Clusters of these the extent in compact bone of those spe- structures may be observed within tuber- cies which do possess secondary osteones cles, crests, and other bony processes. (Foote, ’16; Amprino and Godina, ’47; Their presence in such locations appears Enlow and Brown, ’56, ’57, ’58). A great to be a response to growth circumstances many species lack both the primary and rather than a direct adaptation to tension the secondary osteone, and their bone tis- forces in the traditional sense that “Haver- sues contain primary vascular (non-Haver- sian systems” develop and become oriented sian) canals only. In certain groups, bone in patterns determined by lines of stress. may even be virtually non-vascular. Many Plexiform bone, a basic variation in species possess bone tissues which are the primary pattern of bone structure, composed of mixed bone containing both is rather common in many species, in- primary osteones and primary vascular FUNCTIONS OF THE HAVERSIAN SYSTEM 279 canals. Only a relatively few vertebrate involved, is a structural system involving forms have true secondary osteones as a the deposition of bone within a confined component structure in their bone tissues, space. and even then, their skeleton may con- The distribution of most Haversian bone tain regionally massive amounts of pri- tissues observed in this jnvestigation may mary bone at all age levels. When sec- be accounted for by combinations of (1) ondary Haversian systems do occur, they the primary osteone, (2) the secondary are always found in predictable locations osteone associated with replacement of and patterns of distribution. necrotic bone, (3) the secondary osteone The nature of this distribution makes produced by the compaction of coarse- can- it difficult to explain the function and sig- cellous bone during endosteal growth, (4) nificance of the secondary osteone. Any the secondary osteone concerned with inclusive explanation must satisfy the muscle relocation, and (5) the secondary distribution outlined in the previous para- osteone produced during inward growth graph. involving periosteal resorption and meta- Several conclusions become evident. physeal remodeling. That the utility of the First, the designation of the Haversian osteone extends beyond the developmental system as a universal unit of structure is and functional circumstances recognized unwarranted, even if both primary and in this study is suspected because of the secondary osteones are considered. Sec- inherent versatility of the Haversian sys- ond, one may question the broad generali- tem itself. Studies are now needed on (1 ) zation that the presence and the orienta- specific correlation between aging in bone tion of the Haversian system represent a tissue and corresponding mineral avail- direct adaptation to patterns of physical ability and release mechanisms, (2) bio- stress. Many vertebrate species do not chemical relationships of calcium mobili- possess these structures yet they are sub- zation in the different varieties of bone ject to the same mechanical forces in their tissue, and (3) diffusion or permeability skeleton as forms which do have sec- rates in the calcified bone matrix. ondary osteones. Similarly, mineral re- The non-Haversian canal system in distribution can only represent a partial bone. One of the most widely distributed explanation of the osteone reIative to sec- types of vascular canals in compact bone ondary reconstruction within compact is the simple non-Haversian canal (figs. bone. The observations reported by Am- 1, 3). It is not surrounded by an individ- prino (’52) suggest that secondary recon- ual sheath of concentric lamellae, either struction can be involved in calcium mobil- primary or secondary. This canal type ap- ization, particularly in older individuals. pears in all but a very few vertebrate However, the total absence of secondary groups and at all age levels. It is the typical osteones in numerous species, including canal present, for example, in the cortex many having a long life span, together of the white rat and other laboratory ro- with the characteristic distribution of sec- dents. The non-Haversian canal is found ondary osteones in particular and predic- in widespread areas of monkey compact table relationships and locations when bone and in significant numbers within present in the cortex, indicates that sec- human cortical bone, even in the aged ondary reconstruction is not restricted to skeleton. This canal type, strangely, has this biochemical function. remained virtually unknown to the general Variation in the types of Haversian sys- histologist. The non-Haversian canal is tems. It is apparent that the formation termed simply a “primary vascular canal” of the Haversian system does nut represent in this report to distinguish it from both a single developmental or functional cir- primary and secondary osteones. cumstance. The situation is complex in In view of its extensive distribution in that several varieties of the osteone, as the bone of most vertebrates, and because previously described, exist in compact of its presence in significant quantities in bone. The structure of each, however, is the bone of many common experimental essentially comparable since the osteone animals, an increased recognition of the itself, regardless of developmental factors primary vascular (non-Haversian) canal 280 DONALD H. ENLOW

as a major structural component of bone ging of canaliculi, the spread of necrosis is urged. to adjacent regions of living tissue would Osseous necrosis. The present report be encouraged by the blocking of supply is primarily concerned with the functional channels. The result would be a progres- significance of the Haversian system and sive enlargement of necrotic zones. not with a detailed cytological study of It is evident that necrosis and canal- necrosis in bone. Interest in the process icular calcification are intimately related, of necrosis itself, however, has led to a but a full understanding of the relation- preliminary examination of necrotic bone ship, as well as the fundamental nature at the cellular level. The results of this of osseous necrosis itself, is lacking. work are being continued and expanded as a separate cytochemical study. ACKNOWLEDGMENTS Bone sections containing areas of necrosis This work was supported by the United were stained with oil red 0 in order to de- States Pubic Health Service, Grant D-1123, termine the extent of neutral fat accumu- and by the Upjohn Company. A large lation within osteocytes. Scattered through- number of bone specimens from normal, out compact bone, many individual bone untreated Rhesus monkeys were provided cells were found to contain fatty inclu- by Dr. Paul Ayres, Parke, Davis and Com- sions which largely obscured or displaced pany, Rochester, Michigan. Bone speci- other cytological components. Patterns of mens from monkeys of known age were distribution and tissue relationships, how- supplied by Dr. James A. Gavan, Anatomy ever, were not recognizable with certainty Department, Medical College of South from the preparations at hand. Bone sec- Carolina, and by Dr. G. van Wagenen, De- tion containing necrosis were also stained partment of Obstetrics and Gynecology, with PAS. Differences in the intercellular Yale University. Bone samples from a organic matrix between contiguous living variety of vertebrate forms were provided and necrotic zones were not evident using by Dr. E. T. Hooper and Dr. N. E. Hartweg this procedure. The bone samples exam- of the University of Michigan Museum of ined, however, were from Rhesus monkeys Zoology. having mixed dentition, so that any ne- crosis present must represent a relatively SUMMARY AND CONCLUSIONS recent development. Possible matrix 1. The secondary osteone is regarded as changes in necrotic bone of long standing a structural adaptation to a variety of are not known. functional and developmental circum- A great deal of informstion is needed stances. Secondary Haversian reconstruc- on the metabolic circumstances involved tion is a mechanism which provides inter- in osteocyte death and the resulting in- nal tissue replacement within compact fluence on surrounding intercellular ma- bone yet which does not disturb the gross trix. It is possible that the disappearance form of the bone. of a community of bone cells does not 2. The secondary Haversian system ap necessarily result in an immediate, total pears to be concerned with a process of necrosis of the remaining interstitial tis- replacement or regeneration in areas in- sue in this area, since some interchange volving extensive, natural, non-patholog- between ground substance and collagen ical osteocyte necrosis. with circulating canalicular and lacunar 3. Normal osteocyte necrosis is charac- tissue fluids might survive. This situation teristically associated with particular types may parallel the normal decrease in fibro- of bone tissue structure. Bone varieties blast population within aging connective possessing a sparse distribution of vascu- tissues. A limited distribution of cellular lar canals are most sensitive to the appear- necrosis in bone may be physiologically ance and spread of necrosis. Bone tissues compatible with surrounding areas pos- containing a dense concentration of canals sessing vital cells, but calcareous deposits are more resistant to the onset of necrosis. within communicating canaliculi would 4. A bone is usually composed of sev- subsequently produce a metabolic isolation eral basic varieties of tissue. 'fie distribu- of acellular regions. With continued plug- tion of cellular necrosis in any part of a FUNCTIONS OF THE HAVERSIAN SYSTEM 28 1 bone, or at any age level, can be either the reduction of metaphyseal diameter widespread or restricted to scattered during gross remodeling. patches depending on the distribution and 11. It is emphasized that bone is com- extent of component tissue types which posed of a wide variety of basic bone tissue are more susceptible to necrosis. types, and that each type represents a 5. Bone from very young individuals of structural response to a particular regional certain species, and from all age levels of situation. This important generalization many other species, are composed of must be considered in all experimental densely vascular bone tissues. These and descriptive studies dealing with bone as a tissue. forms do not have widespread cellular ne- crosis, nor do they posses a widespread LITERATURE CITED distribution of secondary Haversian sys- Albinus, B. S. 1757 Academicarum annota- tems in periosteal bone deposits. tionum. 3: 23-24. 6. An increased distribution of resorp- Amprino, R. 1948 A contribution to the func- tion canals and secondary osteones were tional meaning of the substitution of primary by secondary bone tissue. Acta. Anatomica, 5, observed in areas of extensive necrosis. part, 3: 291-300. Secondary reconstruction in periosteal 1951 Relations entre la structure et la bone is not marked when necrosis is con- physiologie de l'os. Ann. SOC.Rouale Sc. Med. fined to scattered, interstitial regiicns. et Natur. de Bruxelles, 4, part, 6: 209-225. 7. A noticeable degree of canalicular 1952 Rapporti fra processi di ricostru- zione e distribuzone dei minerali nelle ossa. I. Calcification has been observed in a sig- Richerche esequite col metodo di studio dell'as- nificant number of bone samples which sorbimento dei raggi roentgen. Seischrift fur display necrosis. The presence of both ex- Zellforschung, 37: 144-183. Barth, A. 1895 Histologische Untersucliungen tensive and restricted necrosis in many uber Knochentransplantationen. Beitr. Path. bones which have not experienced canal- Anat., 17: 65-142. icular calcification, however, suggests Biedermann, W. 1914 Hanclbuch der Verglei- that this process follows rather than trig- chenden Physiologie. By H. Winterstein. gers the fmt appearance of osteocyte Bostock, J. 1825 An elementary system of physiology. Wells and Lilly, Boston, I. death. Detailed relationships between the Broesike, G. 1882 Uberdie feinere Struktur des process of mineral deposition in canaliculi normalen Knochengewebes. Arch. Mikrosk. and with necrosis have not been estab- Anat., 21: 695-765. lished. Bruns, V. 1841 Lehrbuch der Allgenieinen. Anatomie des Menschen. 8. A distinctive type of secondary oste- Cohen, J., and W. H. Harris 1955 The three- one is involved in the compaction of dimensional anatomy of Haversian systems. coarse-cancellous bone during growth re- J. Bone and Joint Surg., 40-.4, No., 2: 419434. versals in metaphyseal-diaphyseal re- Currey, J. D. 1959 Differsnces in the tensile modeling. This variety of the Haversian strength of bone of different liistological types. J. Anat., 93, part, 1: 87-95. system is distinguished by the convoluted 1960 Differences in the blood-supply contours and brecciated construction of in- of bone of different histological types. Quart. terstitial bone located between Haversian Jour. Micro. Sci., 101, 3, 351-370. systems of irregular shape and size. Re- Dempster, W. T., and D. H. Enlow 1959 Pat- construction of necrotic bone is not neces- terns of vascular channels in the cortex of the human mandible. Anat. Record, 135, No., 3: sarily involved in the original formation 189-205. of this type of secondary osteone. Deutsch, C., and Purkinje 1834 De penitiori 9. The hypothesis is advanced that the ossium structura observationes. secondary osteone functions as a muscle Donders, F. C. 1848 Hollandische Beitr. Anat. u. Physiol. Wiss., I. anchoring structure during shifts in the Ebner, V. V. 1875 Uber den feineren Bau der location of muscle attachment produced Knochensubstanz. Bd. der Sitzgsber. Akad. by growth changes and in tubercle drift. Wiss., 111, 72: 49-138. 10. The secondary osteone appears to Enlow, D. H. 1954 A plastic-sen1 method for mounting sections of ground bone. Stain Tech., function as a periokeal and muscle se- 29, 1: 21-22. curing mechanism during the active re- - 1961a Decalcification and staining of sorption of external bone surfaces. Wide- ground thin-sections of bone. Stain Tech., 36, spread periosteal resorption is involved in 4:_. ___950-951 ___. 282 DONALD H. ENLOW

- 1961b A study of the post-natal growth Muller, W. 1926 Uber das verhalten des and remodeling of bone. Am. J. Anat., in Knochengewebes bei herabgestzer Zirkulation press. und das Bild von Nekrose der Zwischenlamel- Enlow, D. H., and S. 0.Brown 1956 A com- len. Beit, z. Klin. Chir., 138: 614-624. parative histological study of fossii and recent Murray, P. D. F. 1936 Bones. Cambridge Uni- bone tissues. Part 1. Tex J. Sci., 8, NO., 4: versity Press. 405-443. Orban, B. J. 1957 Oral histology and embry- - 1957 A comparative histological study ology. C. V. Mosby Co., St. Louis, 4th ed. of fossil and recent bone tissue. Part 11. Tex. Petersen, H. 1930 Die Organe des Skeletsys: J. Sci., 9, No., 2: 186-214. tems. Handbuch der Mikroskopischen Anat- 1958 A comparative histological study ode des Menschen, herausgegeben von V. of fossil and recent bone tissue. Part 111. Tex. Mollendorff. Berlin. Zweiter Teil, 604-616. J. Sci., 10, NO., 2: 187-230. Ruth, E. B. 1953 Bone studies. 11. An experi- Frost, H. M. 1960 In vivo osteocyte death. J. mental study of the Haversian-type vascular Bone and Joint Surg., 42-A,No., 1: 138-143. channels. Am. J. Anat., 93: 429-456. 1960 Micropetrosis. J. Bone and Joint Schwann, T. 1937 Microscopical researches. Surg., 42-A,No. I: 144-150. Sydenham Society, London. Havers, C. Osteologia nova. London. Sherman, M. S., and W. G. Selakovich 1937 1691 Bone changes in chronic circulatory insuffi- Jaffe, H. L., and M. M. Pomeranz 1934 Changes in the bones of extremities amputated ciency. J. Bone and Joint Surg., 39-A: 899% because of arteriovascular disease. Arch. Surg., 901. Smith, J. W. 1960 Collagen fiber patterns in 29: 556-588. mammalian bone. J. Anat., 94, Part, 3: 329- Leeuwenhoek, A. 1678 Microscopical observa- tions of the structure of teeth and other bones. 344. - 1960 The arrangement of collagen fi- Phil. Trans. Roy. SOC.,London, 12: 1002-1003. bers in human secondary osteones. J. Bone 1693 Observations on the texture of and Joint Surg., 42-B,No., 3: 588-605. the bones of animals compared with that of Todd, R. B., and W. Bowmann 1845 The phys- wood. Phil. Trans. Roy. SOC., London, 17: iological anatomy and physiology of man. 838-843. Blanchard and Lea, Philadelphia. Lessing, S. 1846 Uber ein Plasmatisches Gefas- Tomes, J., and C. De Morgan 1853 Observa- system in allen Geweben insobesonders in tions on the structure and development of Kqochen und Zahnen. Hamburg. bone. Phil. Trans. Roy. SOC., London, 143, Mayer, G. H. 1841 Uber die Bedeutung der part, I: 109-139. Knochenkorperchen. Mullers Arch., 210-215. Vigliani, F. 1955 Accriscimento e rinnova- Miescher, F. 1836 De inflammatione ossium. mento strutturale della compatta in ossa Berlin. sotratte alle sollecitajinci ineccaniche. Zeit- Monro, A. 1763 The anatomy of the human schrift fur Zellforschung, 43: 17-47. bones. Edinburgh. Winslow, 3. B. 1734 Exposition of the struc- Muller, J. 1834 Osteologie iind Myologie. Abh. ture of the human body. Translated by G. Berl. Akad. Wiss. Douglas, M. D., London.

PLATE 1

EXPLANATION OF FIGURE

1 Osteocyte necrosis (x) in regions between primary vascular (non-Haversian) canals. Lacunae in necrotic areas lack cells. Shadows appear in some of the empty lacunae and do not represent nuclei. Living cells may be identi6ed by the presence of a distinct darkly staining nucleus. Cells located in close proximity to canals have survived. Femur, Rhesus monkey. 112.5 X. Decalc*ed and stained ground-section. FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 1 Donald H. Enlow

283 PLATE 2

EXPLANATION OF FIGURES

2 Necrosis (x) in a sparsely vacularized zone in circumferential lamellae. Living osteo- cytes are present in those lacunae close to the primary vascular canals. Humerus, Rhesus monkey. 62 X. Decalcified and stained ground-section. 3 Primary, non-Haversian canals in compact bone. Cellular necrosis is absent. This variety of bone tissue is widely distributed in most vertebrate species. It is produced by sub-periosteal apposition of lamellae which enclose primary canals. The individual canals are not surrounded by a broad, tubular sheath of concentric lamellae. Note that these canals are present in varying proportions in many other sections illustrated in this study. Femur, Rhesus monkey. 62 X. Decalcified and stained ground-section.

284 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE a Donald H. Enlow

285 PLATE 3

EXPLANATION OF FIGURES

4 Secondary osteones (A) and resorption canal (B) in an extensive zone of osteocyte necrosis (X). The interstitial lacunae in this zone are all without osteocytes. Dark shadows appear in some of the lacunae due to the thickness of the section and do not represent nuclei. The lacunae of the secondary osteones do contain cells. Osteocytes in the richly vascular zone (D) have not experienced necrosis. Femur, Rhesus monkey. 68.9 X. Stained and decalcified preparation. 5 Enlarged view of the area of secondary reconstruction seen in figure (4) above. The resorption canal (B) has formed within the area of osteocyte necrosis (X). Deposition of concentric Haversian lamellae within such spaces has resulted in the formation of secondary osteones (A) which are now superimposed over the older bone. Note that the lacunae surrounding primary canals (C) in this region are entirely empty of cells. Femur, Rhesus monkey. 106 x. Decalcified and stained preparation.

286 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 3 Donald H. Enlow

287 PLATE 4

EXPLANATION OF FIGURES

6 Resorption canal (A) and secondary osteones (C) located in a restricted region of ne- crosis (x). Note that the lacunae around several of the primary vascular canals are empty (B). Femur, Rhesus monkey. 58 x. Decalcified and stained ground-section. 7 Resorption spaces (A) and secondary osteones in an area of necrosis (x). Femur, dog. 43.5 X. Decalcified and stained ground-section. 8 Haversian bone located in a tubercle. Note the secondary osteone (A) as it enters the previously established compact bone from the external periosteal surface. The lamellar wall of this osteone was continuous with the periosteum. Humerus, Rhesus monkey. 58 X. Decalcified and stained ground-section.

288 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 4 Donald H. Enlow

289 PLATE 5

EXPLANATION OF FIGURES

9 An external layer of small, primary osteones in the formative stage. With subsequent deposition of outer circumferential lamellae, this layer will form a thin “zone” when it later becomes embedded in the cortex. Femur, Rhesus monkey. 62 X. Decalcified and stained ground-section. 10 Necrosis (x) in a circumferential layer of compact bone. Note that the empty lacunae are located in areas which are distant from vascular supply. Femur, dog 62 X . De- calcified and stained ground-section.

290 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 5 Donald H. Enlow -_

291 PLATE 6

EXPLANATION OF FIGURES

11 “Plexiform” bone, a frequent variety of primary bone tissue found in certain vertebrate groups, including some carnivores and most artiodactyls. Mid-diaphyseal section of the femur, transverse section, dog. 56 X. Decalcified and stained ground-section. 12 Secondary osteones in an area of muscle attachment. Note the resorption space (A) in an adjacent zone of necrosis (x). The secondary osteones in the tubercle itself (B) did not form as a response to necrosis. Femur, Rhesus monkey. 56 X. Decalcified and stained ground-section.

292 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 6 Donald H. Enlow

- <- -n -~--~ __- -" --

293 PLATE 7

EXPLANATION OF FIGURES

13 Secondary osteones in an area of muscle attachment. Note that the tubercle is “drift- ing” from side (B) to side (A) and that the secondary osteones (D) and resorption spaces (C) have developed from primary, non-Haversian canals (E) in the direction of the drift. Humerus, Cercopithecus. 57 X. Decalcified and stained ground-section. 14 Secondary osteones associated with endosteal growth. The compaction of coarse- cancellous bone and periosteal anchorage are both involved. Note the irregular con- tours of the interstial bone. Following reversal in direction of growth, outer circum- ferential lamellae (arrows) form a broad zone which now encloses the older endosteal zone. Femur, Rhesus monkey. 57 X. Decalcified and stained ground-section.

294 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 7 Donald H. Enlow

295 PLATE 8

EXPLANATION OF FIGURES

15 Irregular patches of canalicular calcification containing superimposed resorption spaces (B) and secondary osteones (A). Femur, Rhesus monkey. 12.3 X. Ground-section. 16 Necrotic areas involving canalicular caIcification (micropetrosis ) can be identified by their lighter, transparent appearance (A). Femur, Rhesus monkey. 12.3 X. Ground- section. 17 Extensive interstitial micropetrosis between first and second generations of secondary osteones. Tibia, human. 12.3 X. Ground-section. 18 Patches of micropetrosis showing partial replacement by secondary osteones (B). Note the peripheral zone of circumferential micropetrosis (A) and the sparse distribution of canals. Tibia, Rhesus monkey. 12.3. Ground-section.

296 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 8 Donald H. Enlow

297 PLATE 9

EXPLANATION OF FIGURES

19 Secondary osteones in patches of micropetrotic bone in a species from a vertebrate group rarely possessing dense, secondary Haversian tissues. Femur, Gopher Tortoise (Gopherus). 22.8 X. Ground-section. 20 Microradiograph of the same area as (21) below. Note that micropetrosis does not affect the overall density of the interstitial matrix between osteones. 22.8 X. 21 Secondary osteones located within an area of micropetrotic bone. Femur, Rhesus mon- key. 22.8 X. Ground-section. 22 This is the “classic” arrangement of bone tissue structure. A zone of periosteal circum- ferential lamellae (A) encloses two zones of endosteal bone, (B) and (C). Zone (B) is the result of secondary Haversian reconstruction which was involved with inward growth during decrease in the diameter of the shaft. Note the irregular, convoluted contours of the interstitial bone in this area. Zone (C) is composed of inner circum- ferential lamellae. It is the structural result of endosteal deposition which did not in- volve cancellous compaction, since coarse-cancellous trabeculae are reduced in number or absent in the middle third of the diaphysis. Although this particualr arrangement of zones has been traditionally adopted as a standard, representative pattern of bone struc- ture, it is important to realize that many other common patterns of arrangement may be found in compact bone tissue. Femur, Rhesus monkey, mid-diaphyseal transverse section. 57 X. Ground preparation.

298 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 9 Donald H. Enlow

299 PLATE 10

EXPLANATION OF FIGURES

23 Area of muscle attachment in the femur of the Rhesus monkey. Note the concentration of secondary osteones (A) in this specific region. Canals lateral to the tubercle on both sides are primary non-Haversian canals (B). Bundles of Sharpey’s fibers can be seen in the interstitial areas. 20.8 X. Ground-section. 24 Secondary osteones located within patches of micropetrotic bone. Femur, Rhesus mon- key. 72.8 X. Ground-section.

300 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 10 Donald H. Enlow

301 PLATE 11

EXPLANATION OF FIGURES

25 Compaction of coarse cancellous bone during endosteal growth in the metaphysis. Secondary osteones have formed as a result of progressive periosteal invasion of the in- wardly shifting cortex. Humerus, Rhesus monkey. 26.1 X. Ground-section. 26 Resorption canal in experimentally induced necrotic bone (B). Note the deposition of some concentric lamellae within the canal. The external layers of the cortex (A) repre- sent a callus which has enclosed the area of cauterized bone. Femur, white rat. 49.3 X. Ground-section. 27 Progressive formation of secondary osteones during decrease in metaphyseal diameter. Note that the external surface is undergoing resorption, and that the endosteal surface (lower part of the figure) is receiving lamellar deposits. Development of the Haversian systems (A) and resorption spaces (B) has proceeded in an inward direction. The same canals become primary (C) toward the inner third of the cortex. Radius, Rhesus monkey. 69.6 X. Ground-section.

302 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 13 Donald H. Enlow

303 PLATE 12

EXPLANATION OF FIGURES

28 This pattern is produced by inward growth during reduction in metaphyseal diameter. Compaction of cancellous bone is not involved, and endosteal deposits are in the form of circumferential lamellar sheets (A). A broad zone of secondary osteones (B) has de- veloped within the outer part of this endosteal bone. Humerus, Rhesus monkey. 53 x. Ground-section. 29 Following periosteal reversal in direction of growth, the arrangement seen in the pre- vious figure (28) will now have the pattern seen in this section. The zone of secondary Haversian tissue (B), formerly located on the outside of the cortex, forms an inner zone following periosteal deposition of outer circumferential lamellae (A). This ar- rangement is commonly observed in the middle third of the bone. Femur, Rhesus mon- key. 53 X. Ground-section.

304 FUNCTIONS OF THE HAVERSIAN SYSTEM PLATE 12 Donald H. Enlow

305