Scanning Microscopy Volume 1 Number 1 Article 34 10-12-1986 Early Scanning Electron Microscopic Studies of Hard Tissue Resorption: Their Relation to Current Concepts Reviewed A. Boyde University College London S. J. Jones University College London Follow this and additional works at: https://digitalcommons.usu.edu/microscopy Part of the Life Sciences Commons Recommended Citation Boyde, A. and Jones, S. J. (1986) "Early Scanning Electron Microscopic Studies of Hard Tissue Resorption: Their Relation to Current Concepts Reviewed," Scanning Microscopy: Vol. 1 : No. 1 , Article 34. Available at: https://digitalcommons.usu.edu/microscopy/vol1/iss1/34 This Article is brought to you for free and open access by the Western Dairy Center at DigitalCommons@USU. It has been accepted for inclusion in Scanning Microscopy by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. Scanning Microscopy, Vol. 1, No. 1, 1987 (Pages 369-381) 0981-7035/87$3.oo+.oo Scanning Microscopy International, Chicago (AMF O'Hare), IL 60666 USA EARLY SCANNINGELECTRON MICROSCOPIC STUDIESOF HARDTISSUE RESORPTION: THEIR RELATIONTO CURRENTCONCEPTS REVIEWED A Boyde * and SJ Jones Department of Anatomy and Embryology, University College London, Gower St., London WClE 6BT, England (Received for publication June 06, 1986, and in revised form October 12, 1986) Abstract Introduction This paper highlights some observations This paper was presented as the lead-off made by the authors in SEM studies of hard tissue talk at a meeting (Biomineralization: Edward J. resorption and considers their significance in Reith Memorial Meeting on Scientific Investiga­ relation to current concepts. All mammalian tion of Vertebrate Mineralized Tissues) held at mineralised tissues may undergo physiological New Orleans, May 5-7, 1986. This meeting was resorption, the resulting surface reflecting the organized with the purpose of reviewing density of mineralisation and the organic matrix some of the major areas in which the SEM has chemistry, organisation and orientation. contributed to understanding of hard tissue Resorption-repair coupling may follow the structure and function in vertebrates. The resorption of any tissue, but SEM studies first present paper sets out to examine one small facet noted this process in the case of the dental of this microscopic-method-well-suited-to-the­ tissues. The difference between fetal and adult problem area, and from one direction only. We boneformation and resorption provided evidence have taken a second look at our own earlier SEM against the concept of osteocytic osteolysis. SEM data to see how it has affected our viewpoints stereophotogrammetric methods for the quantita­ concerning the natural history of resorption, and tion of individual resorption lacunae are now how the SEM study slots in with other recent cell much quicker and have been extended to the study biological studies. of in vitro resorption by mammalian and avian osteocl asts isolated from bone and seeded into The morphology£!:_ resorption new substrates. Experimental studies using SEM were first The phenomenon of osteocl as tic resorption occurs in all the calcified tissues: not only conducted on the osteotropic hormonal effects on bone, and calcified cartilage, but all the dental bones forming in vivo and extended to the in tissues. The first published SEM study of vitro situation. The effects observed underlined resorption concerned the dentine and enamel of the several actions of PTH on osteoblasts and human deciduous teeth <l>. 3-D images of resor­ indicated their important role in the control of ption surfaces at a range of magnifications bone resorption. Immunological marking techni­ showed that differential rates of removal reflec­ ques monitored by SEM first established that ted local compositional differences in these osteoclasts had no Fe or receptors, although c3 tissues. For example, within the "floors" of other cells in the vicinity did. individual resorption lacunae, peritubular The study of osteoclasts resorbing dentine (PTO) stood proud of the surrounding, substrates other than bone in vitro has increased mineralized-collagen intertubular dentine. In our understanding of the essential components of enamel, prism boundary regions stood above the a resorbable substrate. Experiments growing rest of the enamel structure: at the enamel­ separated bone cells and marrow cells on dentine junction (EDJ), the enamel stood slightly calcified substrates have shown that such cells above dentine (Fig. 1). These studies showed that wi 11 continue to res orb for at least six weeks. the rate of resorption of a hard tissue is influenced by local variations in composition reflecting both the organic matrix chemistry and the density of mineralization (Fig. 2). Referring KEY WORDS:Bone disease, resorption, osteoclasts, to later studies in which it has been surmised osteoblasts, scanning electron microscopy, that collagen breakdown products are chemotactic stereophotogrammetry, enamel, dentine, cementum. for osteoclast precursors <2> and in which the degradation of the collagen has played a major *Address for correspondence: Alan Boyde role in thought processes <3>, we need to Department of Anatomy and Embryology emphasize that osteoclastic resorption can University College London continue in the absence of a collagenous Gower St., London WClE 6BT, England component to a matrix: there is none of this Phone No: 387 7050 (ext 3315) protein in enamel or human PTO. 369 A Boyde and SJ Jones 370 HARDTISSUE RESORPTION figure l. Resorption of human deciduous dentine maturation of the osteoid and its thickness may (top) and enamel prior to shedding a tooth. also be important. Fieldwidth = 296 ,um. The early studies also showed that most figure 2. Rat compact bone o_steocyt~ lacunae human adult bone surfaces entered a "resting" exposed by osteoclastic resorption showing reten­ condition, in which the collagen fibre bundles of tion of separate perilacunar matrix phase, common the matrix were fully mineralized <6, 7,10,12>. in this species. Fieldwidth = 55 ).Jm. Thus intact fibres and bundles could be demon­ figure 3. Human tooth root near apex showing strated in anorganic specimens (Fig. 5). This, patches of resorption and areas_of repair and the fact that much endosteal (Fig. 6) and emanating in prior resorbed areas. Fieldw1dth = trabecular (Fig. 7) resorption occurs in patches 1122 ,um. within fields of well mineralized collagen, figure 4. Horse molar enamel resorbed by osteo­ showed that osteocl asts do not have to contend clasts prior to cementum deposition: another with a barrier of a thin osteoid layer in order example of resorption formation coupling. to recognize real bone <13>. Close examination Fieldwidth = 172 ,um. (Stereo-pair). of our early SfM figures of anorganic prepara­ Figure 5. The lining surface of a Haversian canal tions <6> shows that some endosteal surfaces in adult rat mandible, made anorganic with 1,2 showed nearly, but not quite complete mineraliza­ ethane diamine, showing complete mineralisation tion: some resorption patches can be found ending of matrix surface fibres in this resting surface. within such areas. However, as just pointed out, Fieldwidth = 7. 3 ,A.Jm. some end in osteoid proper. It is obvious that one of the great advan­ Studies of human and other mammalian tages of the SfM is the apparent 3-D nature of cementum resorption <4> showed that some resorp­ the 2-D projection of a surface, making it abun­ tion of the roots of human permanent teeth is a dantly clear as to the morphological complexity perfectly normal occurrence. Indeed, the growth of a resorbing surface. However, a 2-D projection of a second-phase of cementum - which may or may can deceive, and we have always felt the need not contain included cells (cementocytes), but for a real 3-D image in our work. Stereopair which otherwise usually includes a high propor­ images not only convey a vivid impression of tion of extrinsic (Sharpey) fibre bundles - was relationships, but can be formally analysed to shown to occur in relation to small patches of reconstruct profile sections and contour resorption in the apical portion of the root maps <14-16>. We have continued to develop (Fig. 3). This was the first demonstration of stereophotogrammetric methods for the purpose of resorption-formation coupling in an extra­ providing a quantitative description of bone skeletal site. This now popular concept was first resorption <17-19>. proposed for bone on the basis of human metabolic data <5>. (Another dental example of resorption­ formation coupling will be considered later - see Fig. 4 ). Horses have high crowned teeth which erupt The first SEM studies of adult and fetal bone and function before a root is formed. The mecha­ resorption <6, 7> again showed how the nature of nism of tooth attachment is that the crown SEM observations could bring to our attention enamel is covered with cementum, which serves to some important facts. It was found that attach the fibres of the periodontal ligament. resorption lacunae in bone were much srnal ler than This route is adopted by many mammals, but it is in deciduous tooth root removal <B>. It was noted usual for cement to attach to a naturally rough, that osteoclastic resorption left osteocyte pitted surface of enamel. In horses, however, the lacunar walls intact. This observation indicated completed enamel surface, after maturation­ that osteocytes survived until release by mineralization, is superficially resorbed by resorption: they did not themselves remove either osteoclasts (Fig. 4). The reduced, post­ mineral or matrix as was hypothesised in the then maturation ameloblasts have somehow to move or be popular concept of osteocytic osteolysis moved out of the way for this purpose. This <9,10>. Another early SfM finding was that resorption is repaired immediately by the resorbed areas not uncommonly finished within formation of cement. This is another example of fields with mineralizing fronts indicating that resorption-formation coupling. However, this is resorption had occurred into bone covered with most unusual in cement coupling to enamel <20>.