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Functions of the Haversian System

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Functions of the Haversian System 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 bone, 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- osteocyte 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 primary bone 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 bones 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 periosteum 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.
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