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1 of(2013) 10 160–168 European Journal of Orthodontics 35 doi:10.1093/ejo/cjs007 Advance Access publication 26 March 2012 © © The The Author Author 2012. 2012. Published Published by Oxford University Press on behalf of the European Orthodontic Society. All rights reserved. For permissions, please email: [email protected] Re-examination of ‘Einige Beiträge zur Theorie der Zahnregulierung’ (Some contributions to the theory of the regulation of teeth) published in 1904–1905 by Carl Sandstedt Dirk Bister* and Murray C. Meikle** *Department of Orthodontics, Guy’s and St Thomas’ NHS Foundation Trust, London, UK, **Faculty of Dentistry, National University of Singapore, Republic of Singapore Correspondence to: Dirk Bister, Department of Orthodontics, 22nd Floor, Tower Wing, Guy’s Hospital, Great Maze Pond, London SE1 9RT, UK. E-mail: [email protected] The original histological investigation that forms the basis of our present understanding of tooth movement was carried out on dogs by the Swedish dentist Carl Sandstedt at the Karolinska Institute, Stockholm. His findings were published in 1901 as a monograph in Swedish, and shortly after his death in 1904, as three articles in German entitled ‘Einige Beiträge zur Theorie der Zahnregulierung’. Sandstedt observed that the bone was deposited on the alveolar wall of the tension side with both heavy and light forces, new bone spicules following the orientation of the periodontal fibres. On the pressure side, with light forces, osteoclasts resorbed the surface of the alveolar bone, but heavy forces compressed the periodontal ligament resulting in hyalinization—the formation of localized cell-free areas. At these sites, bone removal resulted from undermining resorption by osteoclasts from adjacent marrow spaces. He also observed root resorption and commented on the centre of rotation of the teeth. No English version of Sandstedt’s research has ever been published, and in view of its importance, one of us (DB) has translated his three articles from the original German. The aim was to persuade an orthodontic journal to publish the articles in full—however, weighing-in at 21 000 words, the impracticality of this plan soon became clear. We concluded that excerpts from the text plus commentary would be the most practical solution. Where possible and without materially changing the intended meaning, we have translated the German text into something resembling contemporary English, accompanied by the original 16 figures. SUMMARY Introduction The idea that orthodontic tooth movement is dependent on the resorption and deposition of the bone of the socket dates back at least to 1839 with publication of ‘The Dental Art’ by Chapin Harris (Harris, 1839, p. 104). It was not until the turn of the 20th century, however, that the original histological investigation that forms the foundation of our present knowledge of tooth movement was carried out on dogs by the Swedish dentist Carl Sandstedt (1864–1904). His ndings were published in 1901 (Sandstedt, 1901) as a monograph in Swedish from the Anatomy Department of the Karolinska Institute in Stockholm entitled ‘Några bidrag till tandregleringens teori’ (Some contributions to the theory of tooth movement). Later, three articles in German based on the same work entitled ‘Einige Beiträge zur Theorie der Zahnregulierung’ (Sandstedt, 1904, 1905) which is the source of the present commentary were published in the journal ‘Nordisk Tandläkare Tidskrift (renamed Svensk Tandläkare Tidskrift in 1908)’ shortly after his death (Persson, 2005). As the centenary of the publication of ‘Einige Beiträge zur Theorie der Zahnregulierung’ approached and a review to celebrate the event was being prepared (Meikle, 2006), it transpired that neither of the present authors, we are embarrassed to admit, had ever laid eyes on Sandstedt’s articles, either in the German translation or in the original thesis. In the circumstances, it seemed unlikely that we were alone since as far as we were aware, no English translations of Sandstedt’s research had ever been published. In view of the importance of being familiar with the primary source literature and the origin of ideas, one of us (DB) ‘volunteered’ to translate Sandstedt’s articles into English and make them available to a wider audience. The full translations of Sandstedt’s original publications are available as supplementary material in European Journal of Orthodontics online. In the spirit of Edmund Burke (1729–1797), Irish statesman and philosopher: ‘Those who know nothing of history are destined to repeat it’. Our original aim was to persuade an orthodontic journal to publish the three articles in full—however, weighing-in at 21000 words and written in a rhetorical style that would test the patience of the most dedicated postgraduate student, the impracticality of this plan soon became apparent. We concluded that excerpts from the text plus commentary would be the most practical solution and where possible, without materially changing the intended meaning, have attempted to translate the original German into something resembling contemporary English. It is not clear who was responsible for preparing Sandstedt’s manuscript for CARL SANDSTEDT’ S TOOTH MOVEMENT RESEARCH 2 of 10 D. BISTER AND M. C. MEIKLE 161 40 years not only impeded the progress of tooth movement research for almost 50 years but also the establishment of clinical orthodontics based on sound biological principles. One orthodontist who did recognize the signicance of his work at the time and discussed it in Chapter 8 of his textbook ‘Atlas und Grundriss der Zahnärztlichen Orthopädie’ was Herbst (1910), but the lack of English translations and his premature death meant Sandstedt became the forgotten man of tooth movement research. It was not until 1932 (Schwarz, 1932) when the Austrian orthodontist Martin Schwarz attempted the difcult task of trying to reconcile the differences between the experimental ndings of Sandstedt and Albin Oppenheim (not entirely successfully one might add) in what eventually became the American Journal of Orthodontics that Sandstedt became partially rescued from obscurity and introduced to the English-speaking world. *** Part I: Sandstedt C (1904). Einige Beiträge zur Theorie der Zahnregulierung. ‘Nordisk Tandläkare Tidskrift’ 5, 236–256 Introduction publication, but a rather complex historical review included in ‘Tandregleringens Teori’ (1901) was omitted because of insufcient space. A total of ve plates with 16 gures were included in the three articles but were not accompanied by gure legends. These have been added by the present authors to the best of their ability. All the histological images (Figures 9–16) were hand drawn without magnications and are from tissue blocks sectioned horizontally. Referencing of the gures in the original text is occasionally incorrect. Much of the narrative is in the rst person and one could not accuse Sandstedt of using one word when several would sufce, exhibiting a fondness for particularly long sentences. Nevertheless, in spite of the often turgid prose and the tendency to repeat phrases, it does contain a good deal of what we understand today about the histology of tooth movement. Sandstedt was a man who was clearly ahead of his time and has to be admired for applying the experimental method to what he regarded as a very important problem that ‘nobody had ever thought it worthwhile to investigate’ (pp. 242). There seems little doubt that Sandstedt’s tragic death at the age of The rst paragraph of the Introduction describes the background to the emergence of dentistry from the barber surgeons into a separate profession (p. 236): Orthodontics or the discipline of the regulation of teeth is a relatively new branch of dentistry. Even in the middle of the 19th century, none or indeed very little attention was paid in the orthodontic literature regarding the anomaly of the position of the teeth or their treatment. It is indeed natural that during a time when the activity of a dentist was mainly conned to the extraction of painful teeth or the manufacture of more or less satisfactory tooth replacement, very little importance was attributed to such an unimportant factor as the irregularity of tooth position. But to the same degree that dentistry developed from a surgical craft at the same level as that of a barber to a specic branch within medicine, starting to have a different opinion of the duty of a dentist found wider acclaim. The rich and varied developments that affected all branches of medicine in the latter half of 19th century also paid dividends for the development of dentistry. Scientically minded men, dedicated and zealous, studied purely odontological problems and among the representatives of general dentistry, more and more were interested in scientic research. The darkness that covered a lot of the diseases affecting the dentition lifted gradually and dentistry was provided with new methods as well as new aims and assignments. The following is a footnote on page 236: The dentist Carl Sandstedt passed away as a teacher at the Dental Institute of the Swedish State during the year. The presented article sheds light on a particularly interesting, as well as an unexplored area within dentistry. Unfortunately, the author was not allowed to CARL 162 SANDSTEDT’S TOOTH MOVEMENT RESEARCH nish his work on the theory of the regulation of the dentition. What he has left behind is indeed only a part of his intended work, which nevertheless demands the greatest attention. Pages 238–240: There is a brief description of the deformities affecting the teeth and jaws and how they can be corrected by suitable ‘regulating’ appliances and in the second paragraph various theories of tooth movement: It is clear that every such change of shape of the alveolar process and the jawbones as well as the position of the teeth as outlined in the examples above goes hand in hand with signicant changes to the hard and soft tissues affected by such treatment. A thorough knowledge of the anatomy of those skeletal parts and their tissues as well as the manner in which the changes produced by the operation is indispensable if treatment is to be undertaken in a rational way. The apparatus that is used to straighten or regulate the teeth so that the purpose achieved is a relatively simple task but to undertake the treatment and use it without unnecessary loss of time, unpredictable side effects, unnecessary discomfort, and pain and still achieve the end result, all require a mature assessment and thorough knowledge of the dynamic and physiological principles which underline the movement of teeth. The need for an explanation seems natural; however, it has only been in the last three decades that an important chapter of orthodontics that we call the physiology of tooth regulation has been paid attention to and even to this day, there are a variety of contradictory opinions between various authors on the physiological processes which underlie the movement of teeth. While one group is of the opinion that the movement of the teeth is accompanied simultaneously by new building of bone on one side and resorption on the other side, the other group appears to think that resorption and apposition are completely impossible and that the above changes in the position of the teeth can only be explained by the elasticity of the bone tissue which allows compression and elastic deformation of the spongiosa caused by the operation, which due to changes on a molecular level will eventually equilibrate. Yet, another group of authors takes into account the elasticity of the bony tissues as well as the resorption and apposition processes as they think that the latter would not by themselves be able to explain the speed with which the phenomena, i.e. the movement of the teeth take place. Experimental investigations Pages 241–242: Because I was unable to arrive at a clear view by means of reading the related literature regarding the processes relating to the causes of tooth movement in the jawbones, nor of the dynamic physiological processes, which must regulate the rules of the treatment of orthodontic malformations of the jawbones and the position of the teeth within, I naturally asked myself how to get a clear view among the confusing unproven conceptions. The laws of probability could support both views but none of the above views relied on direct anatomical investigations or brought any D. BISTER AND M. C. 3MEIKLE of 10 other proof. It appeared to me that nobody had ever thought it worthwhile to use investigations during the movement of teeth within the jawbones, to prove or disprove a theory. Walkhoff also points this out, complaining about the lack of it. Mentioning the processes which take place during the straightening of teeth, he remarks: unfortunately, we do not possess any precise anatomical investigations on the changes of the tissues during the movement of teeth. Apart from our own desire to get a clear and determined view of one of the most important questions on the subject in orthodontics, it was also mainly the statement of Walkhoff, which prompted me to start the experimental investigations on which I am about to report. Friedrich Otto Walkhoff (1860–1934) was a dentist from Brunswick in Germany who in 1901 published an atlas on the anatomy and histology of teeth and their supporting structures entitled: ‘Die normale Histologie menschlicher Zähne; einschliesslich der mikroskopischen Technik’. Following Roentgen’s discovery of x-rays in 1896, Walkhoff is credited with taking the rst dental radiograph—of his own teeth with an exposure time of 25 minutes. The remaining sections of Part I are concerned with the reason he chose dogs for the experiments: ‘without much hesitation I decided on the dog’, plus descriptions of the appliance used to move the teeth, and the use of plaster models and radiographs to measure the amount of tooth movement. The methods of xation, decalcication, and embedding of tissue blocks taken from the jaws as well as the preparation of stained histological sections cut in the horizontal and sagittal plane are discussed in considerable detail. Measurements of the amount of tooth movement were made from both plaster casts and radiographs. Page 250: During the rst experiments, I used a very simple but equally satisfactory apparatus. This consisted of a brace, which followed the labial surface of the upper front teeth exactly and consisted of rings (bands) and caps, which were cemented to the canines. Rings were cemented on the labial surface of the canine with horizontal tubes through which the brace ran. The ends of the latter were applied with a ne thread and tail ends were xed with a screw–nut. Plate I (Figure 1) shows such an apparatus that is still xed to a previously sacriced animal. Due to the design of the apparatus, it was a relatively simple task through slow tightening of the screw–nuts to produce a movement of the upper front teeth to the palatal plane, with the canine teeth moving anterior along the line of the arch. . . . To get a better idea about the dimension of the changes, which were induced by the apparatus on the alveolar process, I took impressions of the jaws before and after the experiment (Plate II; Figures 3 and 4). For one experiment in which I managed to get two identically sized dogs which came from the same litter, I managed to take photographs as you can see in Plate I: one dog was used as the experimental dog and the other as a control. From these photographs, one can see the apparatus used and the changes produced in the position of the teeth. The front teeth of the upper jaw in the experimental animal CARL SANDSTEDT’ S TOOTH MOVEMENT RESEARCH 4 of 10 D. BISTER AND M. C. MEIKLE 163 Plate I [Sw: Plansch] Photographs of the control (1) and experimental (2) dogs at sacrice. The mandibular canines were removed to allow movement of the maxillary teeth. The appliance consisted ofan archwire inserted into tubes attached to bands on the canines; distal to the tubes was a screw mechanism, which when tightened, moved the incisors lingually and the canines mesially. (Figure 2) show the above mentioned position bite against the lingual surface of the opposing teeth in the lower jaw. In the control animal (Figure 1), this relationship is normal. Page 251: Apart from these photographs, I have in all experimental and control animals, taken radiographs of the anterior parts of the jaws apart from the rst animal used in the experiment. These radiographs on Plate II (Figures 5–8) show particularly well and better than all descriptions, the signicant changes in the anterior part of the alveolar process, and the position of the teeth produced by the experiment. *** Part II: Sandstedt C (1905). Einige Beiträge zur Theorie der Zahnregulierung. ‘Nordisk Tandläkare Tidskrift’ 6, 1–25 The rst experiment Design of the experiment Page 1: The rst experiment was conducted with a 14-month-old male dog of undetermined pedigree. On 28 November 1899, two lower canine teeth were fractured trying to extract them. Two days later, the above-described brace was xed. Due to daily tightening of the screw–nut, I achieved the movement of the incisal teeth palatally with the canine teeth moving forwards along the line of the arch. At Plate II Study models and radiographs used to document the amount of tooth movement. Left: control and right: experimental dogs. The experiment lasted 3 weeks and during that time, the crowns of the incisor teeth moved approximately 3 mm palatally. (The X-rays of the day, referred to as skiagrams, produced a positive image, not the negative image of contemporary radiographs.) the time of the dog’s sacrice after 3 weeks, the upper front teeth had moved palatally to such a degree that they contacted the lingual faces of the opposing teeth in the lower jaw. We took impressions of the jawbone. The lower jaw was sectioned into two parts after all soft tissues had been removed. On one mandibular half, we used a section just anterior to the premolar. Equally, the upper jaw was sectioned in the midline. Histology Pages 2–7 are concerned with a detailed description of the structure of alveolar bone, the periodontal ligament, and the location of osteoblasts on the surface of the cementum and alveolar wall between Sharpey’s bres. At the time, the name for the periodontal ligament had not been settled upon. In D. BISTER AND M. C. 5MEIKLE of 10 CARL 164 SANDSTEDT’S TOOTH MOVEMENT RESEARCH the original text on page 4, Sandstedt says: ‘the space between the alveolus and the tooth is occupied by a brous sturdy tissue that was given the most varied names by individual authors, such as ‘Wurzelhaut (skin of the root)’, ‘Wurzelperiost (periosteum of the root)’, ‘Pericement and AlveoloDentalmembran among others’. He then continues ‘Die Wurzelhaut’ without giving a reason why he chose this term in particular. Later on, he uses ‘Wurzelperiost’ and these are the two most commonly used ones in the text. The role of osteoclasts in the development and growth of bone is described in order to understand how these cells relate to changes in the tissues during tooth movement—the rst reference in the literature to hyalinization of the periodontal ligament (PDL) is on page 10 and undermining resorption of the adjacent bone by osteoclasts is on page 11. The rst description of root resorption associated with orthodontic tooth movement is on page 22. Page 2: To get a clear impression of the manner and quality of the changes which have been caused by orthodontics, it is necessary to recall the normal structures which are involved when moving teeth inclusive of their surrounding tissues, namely, apart from the teeth themselves, the periodontal ligament of the tooth, the alveolar process and the periosteum of the latter. Pages 7 and 8: After this short review on the normal structures of the tissues, which are more or less affected by the movement of teeth, I will now give a more detailed description on the observations, which I gained through sections of the rst series of experiments. To highlight the details of the relevant changes individually, it should be appropriate to choose the most instructive sections and describe them in detail. For this purpose, I will show the following: 1. Horizontal section through a piece of the alveolus on the right side of the upper jaw, which contains the roots of the canine and the rst premolar. 2. Horizontal section through the anterior segment of the left side of the upper jaw, which contains the roots of the incisors and half of the root of the canine. Pages 8 and 9: The following is a description of the changes associated with the forward movement of the right canine: We only nd something really remarkable on the distal aspect of the alveolar wall. This is not as the usually described lamellar bony structure consisting of regular arches building a border to the alveolus but instead consists of irregular beams (trabeculae) strips of a light-gleaming bony substance. Between and within the lamellae, we also observe larger and smaller completely enclosed hollows or encapsulations, which are lled with cell-rich connective tissue. Even under low magnication, it is unambiguous that there is periosteal bone deposition (Plate III; Figures 9 and 10). Larger magnication allows us to look into the process in more detail (Plate IV A: Figure 11). The newly laid bony depositions arranged radial to the wall and at right angles show particularly clearly characteristics of crude bony tissue. Numerous large and irregularly built bony lacunae lie densely packed without any clear structure within the bony substance, which itself is perforated by Sharpey’s bres, the direction of the latter representing clearly the direction of the lamellae of the original wall. The border between the latter and the newly built alveolar wall is clearly demarcated in the von Ebner ’s cement (reversal) line (Plates III and IV A and B). Page 10: On the buccal alveolar wall, however, there is very active resorption in progress. The periodontal ligament is completely detached on a rather large area, which itself shows the same irregular porous morphology which characterizes Howship’s lacunae in the resorption areas. Wherever the osteoclasts are starting to destroy the walls of the alveolus, they tear apart the connection between Sharpey’s bres and the connective tissue within the periodontal ligament. It is only where osteoclasts appear in a closed bulk that we observe the completely disconnected periodontal ligament. Apart from the posterior half of the buccal wall, there is also a demarcated resorption process on the anterior palatal wall. The osteoclasts have completely broken down the part of the wall that separated the alveolus from the surrounding marrow and are now busy undermining (Ger: untergraben) the residual part of the original alveolar wall. Page 11: . . . the existing periodontal ligament also has a very different appearance. In low magnication, it appears to have a homogenous, white and shiny appearance (Ger: homogenes, weisses, glänzendes Feld) in which we distinguish individual light blue coloured speckles or small blue bands, but no other elements that we normally nd in the periodontium. Even in larger magnication, we cannot nd nuclei. They seem to have disappeared altogether or they seem to have lost their ability to stain. The above-mentioned blue speckles or stripes can be interpreted as residues of tissue walls or nerves. Also, the typical brillary structure is lost and has been replaced by a regular homogenous substance (Ger: homogene Substanz) pierced by shiny cracks (Plate IV A: Figure 12). It is quite clear that what we see is a product of the residual degeneration, a hyalinization of the soft tissues, a sclerotic periodontium in which we now see regenerative processes (ein Degenrationsprodukt, eine Hyalinumwandlung des Bindegewebes, eine sklerosierte Wurzelhaut). Sandstedt subsequently used ‘hyaline Substanz’ and ‘hyalines Bindegewebe’ (hyaline connective tissue) interchangeably. *** Part III: Sandstedt C (1905). Einige Beiträge zur Theorie der Zahnregulierung. ‘Nordisk Tandläkare Tidskrift’ 6, 141–168 The second experiment Page 141: The results from my rst experiment appear to be quite satisfactory. It gave me good insight into the processes, CARL SANDSTEDT’ S TOOTH MOVEMENT RESEARCH 6 of 10 D. BISTER AND M. C. MEIKLE 165 Plate III Horizontal sections through the right maxillary canine; the direction of movement is towards the top. Figure 9 is a section cut in close proximity to the alveolar rim. (A) At the site of presumptive compression, the periodontal ligament (PDL) shows the glassy appearance characteristic of hyalinization, with osteoclasts undermining the adjacent alveolar wall. (B) On the buccal side of the root, a thin layer of lighter staining new bone is demarcated from the old bone by a von Ebner ’s (reversal) line. At the bottom, new bone takes the form of lighter staining bony trabeculae of woven bone orientated in the direction of pull. (C) On the right side, osteoclasts are resorbing the alveolar wall; on the left, the detachment of the PDL from the bone is the result of a tear during sectioning. Figure 10 is a section through the middle third of the same tooth. (In dogs, the pulp canal expands towards the middle third of the root before narrowing towards the apex.) General remodelling activity at the bone–PDL interface is seen, but evidence of the accelerated bone formation and resorption is absent. This area corresponds to the centre of rotation of the tooth. which appear in the surroundings of the regulatory apparatus of the teeth, which are inuenced by it. It appears, beyond doubt, that the changes in the position of the teeth which are caused during the operation (the force application during xed appliance treatment) are inuenced at least to a large extent by resorption and apposition, which are in direct connection with the pressure and tension and cause the movement of the teeth. Sandstedt then goes on to compare the tissue changes introduced by experimental means with the corresponding parts of the alveolar process in a control animal. The jaws were sectioned in both horizontal and sagittal section and the description of the changes he observed occupies several pages. Much of it is repetitive, but does include the rst references to the centre of rotation of the teeth being near the middle of the root (pages 153 and 157), as well as a description of root resorption (page 160). Page 157: The intensity of resorption and new bone formation appeared directly proportionate to the amount of pressure and tension. In the areas of the alveolus where the effects were not as prominent, such near the middle of the root, there was relative quiescence; apposition and resorption were less vibrant here (see Plate III; Figures 9 and 10). The largest intensity of those processes was in the proximity of the alveolar rim and close to the tip of the root. . . . Occasionally, it was demonstrated that the resorption process started in the bone marrow cavity and developed signicant intensity there, while the alveolar wall was still intact. This appeared to be continuously repetitive in areas where the alveolar wall was covered by periodontal tissue, which had become sclerotic. Page 160: In all the investigations that I have undertaken so far, in only two cases, could I demonstrate a pathological change of the tooth itself. The rst case was demonstrated in series 2 (described in Part II, page 21) where the tip of the root of the second incisor was strongly overgrown (Ger: usuriert), so that it was embedded in signicant inltration tissue. It is very likely that the tooth was in this case exposed to strong pressure, apart from the pressure, it was exposed to by the regulatory apparatus . . . It was demonstrated that the intensive resorption process (Ger: der intensive Resorptionsprozess) . . . attacked the tooth itself and caused a defect in it, which extended deeply into the tooth structure itself (Plate IV B: Figure 14). These resorption processes are as already known, a constant returning feature to roots CARL 166 SANDSTEDT’S TOOTH MOVEMENT RESEARCH D. BISTER AND M. C. 7MEIKLE of 10 Plate IV A: These sections show at a higher power the cellular and tissue changes in the periodontal ligament (PDL) and bone at sites of presumptive tension and compression. Figure 11: Tension (B) newly laid down woven bone with vascular spaces clearly demarcated from the older lamellar bone, (C) highly vascular PDL, (D) cementum, (E) dentine. Figure 12: Compression (A) bone of the original alveolar wall, (B) numerous darkstaining osteoclasts lining the bone surface, (C) the PDL in which the brillar stucture has been lost and replaced by a glassy homogeneous or hyalinized tissue, (D) cementum, (E) dentine. Plate IV B Figure 13: Direct resorption. (A) periodontal ligament (PDL) at a compression site showing its normal brillar appearance. (B) Numerous multinucleate osteoclasts in Howship’s lacunae are resorbing the surface of the bone. (C) Cortical bone of the alveolus; two Haversian systems or secondary osteones are clearly visible. Figure 14: (A) PDL with hyalinized PDL. (B) Although one cannot be absolutely sure, this section was likely to have been included to represent resorption of the root cementum at (C) by multinucleate giant cells. of temporary as well as retransplanted and transplanted teeth. That these occurrences appear on teeth that have been under the inuence of a regulatory apparatus I assume is extremely likely. Page 164: Summarizing the above observations, we now nd that the periodontal ligament in the areas of the alveolus where new bone formation is taking place, has a normal appearance, but that this appearance under the inuence of larger or lesser pressure undergoes more or less signicant changes depending on the amount of pressure it is subjected to. Relatively moderate pressure, as it is usually found during orthodontic treatment, results in only little inammatory reaction of the periodontal ligament and subsequent atrophy of the alveolar wall. If however the pressure increases to such a degree that persistent circulatory disturbance is caused, the pressure will cause deeply degenerated changes of the periodontal ligament which either lead to gradual death or to quick necrosis of the tissue. But the disturbance of the circulation is not only conned to the periodontal ligament but also causes serious disturbances of the circulation in the surrounding parts of the alveolar process. That this is the case can be best demonstrated by the consistent thrombosis of the vessels. Sandstedt ends Part III by discussing the possible role of bone bending in tooth movement. This had been proposed by Kingsley (1880), based on observations made while treating prognathic bites that tooth movement was due to the exibility of the alveolar bone. Much of the argument is not easy to follow, but Sandstedt does appreciate the difculty of demonstrating bone bending experimentally. CARL SANDSTEDT’ S TOOTH MOVEMENT RESEARCH 8 of 10 Page 165: Regarding the second particular issue in the programme of my investigation, in how far apart from the above above-mentioned processes, there is also compression and stretching of the cancellous bone, and if this was the case whether purely interstitial changes take place, I am not able to answer unequivocally at this stage. . . . That the alveolar structures in young individuals are extraordinarily pliable should be as I already mentioned earlier without any doubt, but in how far, this exibility plays a role during tooth movement is a different matter. The observations, which I made during my rst experiments, do not in any way support such a theory. I was indeed fully aware, even before my rst investigations began of the difculties which I would encounter attempting to investigate such changes histologically. A nearly satisfactory resolution of these questions can only be derived at by way of experimentation in such a way that quick and signicant remodelling of the alveolar process can be affected that would be impossible to be caused by resorption and apposition (Plate V; Figure 15 and 16). D. BISTER AND M. C. MEIKLE 167 applied force, or how far the teeth were moved. The time course of the experiments was 40 days at which point the animals were sacriced. Space does not permit a full evaluation of all the experiments described in the paper by Oppenheim (1911), but he concluded that bone reacts to pressure by a transformation of its entire architecture. This he believed occurred by resorption of the existing bone and Postscript The enduring question, bearing in mind that both the illustrations and the descriptions of tooth movement quoted above are ones we would recognize today, is why Sandstedt’s research languished in obscurity for so many years? His premature death and publishing in Swedish and German certainly played their part but are not the whole story. At this point, Edward Hartley Angle enters the narrative. In 1911, the Viennese orthodontist Albin Josef Oppenheim (1875–1945), published his famous article entitled ‘Tissue changes, particularly of the bone, incident to tooth movement’ in the Transactions of the European Orthodontic Society, forerunner to this journal. Oppenheim’s research was brought to the attention of Angle who invited him to give a series of lectures at the Angle School, at the time located in New London, Connecticut. Oppenheim clearly made an impression, his theories being enthusiastically endorsed by Angle, and members of the Angle Society. Oppenheim rejected both the pressure–tension hypothesis supported by the histological evidence of Sandstedt and the theory of bone bending advanced by Kingsley (1880) based on the elastic properties of bone. To explain his ndings, Oppenheim proposed an alternative: The Law of Bone Transformation, in which the alveolar bone was completely reorganized in accordance with Wolff’s Law (1892). Oppenheim carried out his experiments on the lower deciduous incisors of baboons, although it is not clear exactly how many animals were involved. The tooth movements reported were labial, lingual, depression, elongation and rotation—one half of the jaw being operated upon and the other half being used as an internal control; the paper fails to include either a description or an illustration of the orthodontic appliances used, the magnitude of the Plate V Figure 15: Sanstedt used this image to exemplify septum displacment between two teeth caused by orthodontic forces and shows the appearance of the tissue in those areas with signicant resorption, close to the tooth the periodontal ligament (PDL) still shows some hyalinization. The clear areas are likely to be processing artifacts or tears produced while sectioning. (A) Dentine with small zone of hyalinized tissue adjacent to it, (B) disorganized PDL tissue, (C) remnant of bone with several osteoclasts, (D) Haversian system surrounding a large blood vessel, (E) lipid droplet in marrow cavity, (F) likely to be aggregates of lymphocytes and plasma cells, (G) multinucleate giant cells resorbing hyalinized tissue. Figure 16: Horizontal section of the bone between adjacent teeth. (A) Dentine, (B) PDL, (C) newly deposited bone clearly demarkated from the darker staining old bone. D. BISTER AND M. C. 9MEIKLE of 10 CARL 168 SANDSTEDT’S TOOTH MOVEMENT RESEARCH its replacement by new bone, both processes occurring simultaneously until nally deposition preponderates over resorption. He emphasized that bone transformation occurred only with very light physiological forces; should the applied load be excessive the result was vascular occlusion and damage to the PDL and supporting tissues. It is therefore noteworthy that Oppenheim was unable to conrm Sandstedt’s observations regarding hyalinization of the PDL and associated undermining resorption. In view of the later ndings of Reitan (1957) that hyalinization of the PDL occurred in human subjects with forces as low as 30 gm (0.3 Newtons), this suggests the forces Oppenheim applied to the teeth were very light indeed. In fact, Oppenheim’s illustrations bear more than a passing resemblance to the trabeculation of alveolar bone observed at the bone—PDL interface in a rat model of tooth movement—the result of stress shielding of the tooth supporting structures by the presence of an orthodontic appliance activated or otherwise (Milne et al., 2009). Interestingly, although Oppenheim rejected the pressure– tension hypothesis, he still refers to the side of pressure and the side of pull and regarded his experiments as indubitable refutation (sic) of the pressure theory. There is also a certain amount of ambiguity in his attitude to bone bending and it is apparent that he recognized the elasticity of bone and the role that property might play in tooth movement, particularly in children and young adults. Finally, since he was of the opinion that the fulcrum of movement was at the apex of the tooth and having found bone formation and bone resorption on both sides of the teeth, it is unclear precisely how Oppenheim thought teeth were moved into a new position. In retrospect, Oppenheim’s theory of bone transformation made such little sense it’s surprising that anyone believed it. Be that as it may, the theory did seem to support Angle’s non-extraction philosophy and the widespread belief at the time that orthodontic appliances could ‘grow bone’. More importantly, Oppenheim remained research active and continued to publish in German and English language journals up until the time of his death in Los Angeles, having managed to escape from Austria in 1938 following the ‘Anschluss’ (Atkinson, 1957). He also had the support of many inuential pupils of Angle including Frederick Noyes, Professor of Histology and Orthodontics, and later Dean (1924–1940) of the College of Dentistry, University of Illinois Chicago. In a posthumous tribute to Oppenheim’s research, Noyes (1945) was contemptuous of the ndings of other workers, writing in a rather pejorative tone: ‘one investigator thought that the bone was bent and another that the tooth plowed (sic) through the substance of the bone by means of absorption on one side and deposit on the other ’. The latter comment presumably a reference to Sandstedt. With the centre of gravity of orthodontics becoming rmly embedded in North America during the 20th century, the outcome was that Oppenheim’s research appeared in mainstream English language textbooks to the exclusion of all others (if any reference to the histology of tooth movement appeared at all), until the aftermath of World War II and the expansion of university-based orthodontic training programmes—a salutary reminder of how ideologies or dogmas can become entrenched by powerful and dominant personalities. The problem of course with ideologies is that they provide all the answers—lack of evidence or evidence to the contrary is completely irrelevant. In closing, it is therefore perhaps worth bearing in mind the motto of the Royal Society of London, founded in 1660 to promote scientic research and discussion: ‘Nullius in verba’—‘Nothing upon another ’s word’. Supplementary material Full translations of Sandstedt’s original publications are available as supplemental material in European Journal of Orthodontics online. References Atkinson S R 1957 Orthodontic proles: Albin Oppenheim. American Journal of Orthodontics 43: 46–51 Harris C A 1839 The dental art. A practical treatise on dental surgery. Armstrong and Berry, Baltimore Herbst E 1910 Atlas und Grundriss der Zahnärztlichen Orthopädie. Verlag von J F Lehmann, Munich Kingsley N W 1880 A Treatise on Oral Deformities as a Branch of Mechanical Surgery. D Appleton and Company, New York Meikle M C 2006 The tissue, cellular, and molecular regulation of orthodontic tooth movement: 100 years after Carl Sandstedt. European Journal of Orthodontics 28: 221–240 Milne T J, Ichim I, Patel B, McNaughton A, Meikle M C 2009 Induction of osteopenia during experimental tooth movement in the rat: alveolar bone remodeling and the mechanostat theory. European Journal of Orthodontics 31: 221–231 Noyes F B 1945 The contribution of Albin Oppenheim to orthodontia. Angle Orthodontist 15: 47–51 Oppenheim A 1911 Tissue changes, particularly of the bone, incident to tooth movement. Transactions of the European Orthodontic Society 303–359. Reprinted 2007 European Journal of Orthodontics 29: i2–i15 Persson M 2005 A 100th anniversary: Sandstedt’s experiments on tissue changes during tooth movement. Journal of Orthodontics 32: 27–28 Reitan K 1957 Some factors determining the evaluation of forces in orthodontics. American Journal of Orthodontics 43: 32–45 Sandstedt C 1901 Några bidrag till tendregleringens teori. Kungl Boktryckeriet. P A Nordstedt & Söner, Stockholm Sandstedt C 1904 Einige Beiträge zur Theorie der Zahnregulierung. Nordisk Tandläkare Tidskrift 5: 236–256 Sandstedt C 1905 Einige Beiträge zur Theorie der Zahnregulierung. 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