Intraosseous Anchorage of Dental Prostheses

An Early 20th Century Contribution

Robert J. Rudy, DMD; Paul A. Levi, Jr, DMD; Fred J. Bonacci, DMD; Arnold S. Weisgold, DDS; Daniel Engler-Hamm, DMD, Dr. Med. Dent., Msc

Throughout history, humankind has appreciated the value of teeth and has sought ways to replace them.¹ However, it is only within the past 200 years that members of the dental and medical professions have made substantial progress in the permanent replacement of missing teeth by intraosseous anchorage of artificial metal fixtures. The first case report dates back to Maggiolo in 1809,^2,3 in which he described implanting gold roots. Several case reports followed on the implantation of artificial materials to allow tooth replacement by Rogers (1845), Younger (1885), Edmunds (1886), Harris (1886), Bonwill (1895), Edwards (1889), Payne (1898), and Schnol (1905).^2,3 There are many reasons for failure of these early advances; however, perhaps the most significant reason is that in the 19th century iron, gold, lead, and porcelain were used either to replace teeth as artificial roots or as a coating for a replanted or transplanted tooth.^4-7 These materials were not biocompatible, and thus, caused early bone resorption and subsequent implant failure.

By 1913, implantation, transplantation, and replantation were mentioned together in referenced indices. Implantation referred to implanting a synthetic or natural tooth, transplantation described removing a natural tooth from one area or person and placing it in another site or another person, and replantation described removing a tooth and replacing it in the same site. The majority of articles, however, dealt with the replantation and transplantation of natural, not artificial, teeth. Thus, by 1913 significant knowledge existed on the replantation and transplantation of natural teeth, but very little information was available on the placement of artificial implants.^8,9 Greenfield, who graduated in 1899 from the Chicago College of Dental Surgery and practiced in Wichita, Kansas, recognized the limitations of natural tooth implantation and started experimenting with the implantation of artificial hollow-cylinders made of iridoplatinum wire soldered with 24 karat gold. This “hollow basket” design was very similar to the design adopted many years later by the Straumann Group (Basel, Switzerland). Greenfield patented his idea in 1909, nearly 100 years ago, and he first reported on this concept in 1911.10 He then presented a very detailed description of his experience and methods before the Academy of Stomatology in Philadelphia on January 28, 1913. His lecture was published in Dental Cosmos, a highly respected dental journal at that time.¹¹

The authors feel that the value of Dr. Greenfield’s presentation should be more widely recognized because the basic principles and surgical techniques that he used 100 years ago are very similar to those used today. This paper will illuminate Greenfield’s work and compare his and other pioneers’ significant contributions with the contemporary practice of implant dentistry.

MATERIAL AND METHODS

The authors conducted a Medline® search on the history of endosseous implants (Tufts University, Health Science Library, Ovid Medline 1966-2006, January 5, 2007). The following searches were performed: (1) “history endosseous implant;” (2) “history dental implant;” (3) “dental implant;” and (4) “endosseous implant.” Because the body of literature was too extensive for the third and fourth searches, another set of searches limited to review articles was performed and 186 articles were found. A review of these articles resulted in 42 relevant articles about implant history or major implant innovations or contributions. The authors found very limited information on the history of dental implants because the majority of the articles reviewed implant surfaces, shapes, materials, osseointegration, or dental implant treatment planning. Thus, the authors reviewed the references of the obtained articles and searched for articles by Brånemark, Linkow, and Schroeder by hand because these individuals seemed to have influenced implant history significantly (Table 1).

Their early works were obtained and their references reviewed, which unveiled further pertinent information on historical landmarks in implant dentistry. Several articles from the early 20th century were obtained and reviewed, and their importance was ranked based on today’s understanding of implant dentistry. As part of the review process, the authors discovered Greenfield’s original 1913 article. Because of the detailed implant-related descriptions within the article, the authors began to review the background of knowledge that Greenfield must have had in 1913. As a result, American dental textbooks and the national dental literature indexes from 1890-1925 were reviewed. Also, the orthopedic surgical literature provided the authors with information on several advances in regard to the use of metals in surgery and the knowledge in performing orthopedic surgery around 1913. To provide historical context to Greenfield’s surgical procedure, the authors’ research team collected literature that pertained to any advances in local anesthesia, sterilization of instruments, aseptic and antiseptic surgical techniques, and the implantation of natural teeth.

RESULTS

Several review articles have been written regarding the history of endosseous implants;^1-7,12-15 however, none of these articles focuses on those who pioneered the most significant developments in implant dentistry, and how these contributions relate one to another. The authors of this article discuss the following topics and their historical background together with the main contributors of each topic:
I Materials and osseointegration I Design and loading
I Surgical technique
I Surface

MATERIALS AND OSSEOINTEGRATION

By the end of the 19th century, the groundwork was laid for the advances that were to follow in the field of dental implantology. Sterility of instruments and antiseptic/aseptic principles of wound management already had been developed for general and orthopedic surgery.^16-24 X-rays were discovered in the winter of 1895 in Germany, and their application through radiography quickly followed in the fields of medicine and dentistry in the early months of 1896.^25,26 The introduction of local anesthesia in 1885, by William Halstead, provided dentists with the opportunity to experiment with the implantation of natural teeth.^17,18,27,28 By 1913, numerous publications on implantation had been written.^8,9,29,30

It remained for Greenfield to realize the shortcomings of using natural teeth (slow to rapid root resorption) and to embark on clinical research using a metal substitute. It was his hope that because these metal root substitutes would not resorb, they would provide a long-lasting artificial platform, anchored in healthy bone, upon which to build dental crowns and bridges.^10,11,31 It was the chance observation of an orthopedic operation, in which silver wire suture was used, that prompted Greenfield to consider the use of metal in the placement of endosseous dental implants.11 He envisioned that the metal would be well tolerated by the bone and gingival tissues of the partially edentulous jaws of his patients. The surgical use of silver wire was already well known in the treatment of gynecological problems. Pioneering work by Marion Sims in America and Montague Gosset in England proved that this metal suture was well tolerated by the soft tissues in the successful closure of vesicovaginal fistulas.^32-35 Also, in 1875, Hugh Owens Thomas of Liverpool, England, described the successful use of silver wire to stabilize the reduced fragments of a fractured mandible.³⁶

In 1924, Arthur A. Zierold, a surgeon from the University of Minnesota, undertook a research project using dogs, where he compared the tissue reaction to aseptic surgical implantation of several different metals.³⁷ The objective of his research was to determine whether metal, when implanted into living bone, exerted an influence other than that of any foreign body; and if so, whether this was a property common to many metals or did the reaction vary with each individual metal. Using 63 mature dogs, Zierold implanted the following metals into different skeletal regions: gold, silver, aluminum, zinc, lead, copper, nickel, high carbon steel, stellite, magnesium, iron, and copper aluminum alloy. After a 2- to 6-week healing period, the dogs were sacrificed and histologic specimens obtained. This was one of the first studies that used histologic techniques to help confirm clinical impressions of biocompatibilty.

Though Zierold did not find fusion of bone tissue to any of the metal implant surfaces, it was apparent that different metals exhibited different types and degrees of tissue reactions. Some of his observations were that: (1) gold, aluminum, and stellite were readily tolerated by bone and tended to be encapsulated with fibrous tissue; they were inert materials, unaffected by the living cells and body fluids; (2) silver and lead were slightly less tolerable to bone, but they easily underwent corrosion, and created a greater connective tissue response; (3) zinc corroded easily and caused a slight connective tissue reaction; (4) copper caused definite stimulation of bone, although it underwent slow corrosion; (5) steel and iron definitely inhibited bone regeneration and steel readily underwent corrosion. Zierold speculated that the process of corrosion of the metals in body fluids played a significant role that would explain the different tissue reactions to the various metal implants. Overall, Zierold wrote that his observations coincided with those of a French researcher, Le Fort, whom he quoted: “When the mass is nonseptic, nonirritating by its anatomic location or form or chemical nature, the organism tends to ignore it and the phenomena of defense do not appear. The usual reaction is the encapsulation in a dense wall of fibrous tissue.”³⁷

Expanding on this research, San Antonio, Texas, surgeons Venable and Stuck published a series of articles from 1936- 1938,^38-40 in which they researched corrosion as the main cause for the lack of biocompatibility. The metal that was found to exhibit the least degree of corrosion was vitallium, a mixture of cobalt, chromium, and molybdenum. They stated: “We feel that the criterion in the matter of osteosynthesis with metals is that the metal must be electrically neutral or entirely passive in the presence of body fluids and significantly rigid and strong to do its part mechanically. Surgeons are fortunate in having this metal....”³⁸

In 1939, A. E. Strock of the Harvard School of Dental Medicine was the first clinician to use a screw made of vitallium in a human extraction site.⁴¹ This electrically inert material allowed, for the first time in the history of implantation, a reaction-free recipient site after surgical implantation.^42-45 Strock later placed a prosthetic dental crown on this vitallium screw. Unlike Greenfield, who believed that the stability of the implant related to the “locking” of bone in and around the hollow basket design and to the surface of the metal itself, Strock believed that the “principle of the screw” was responsible for clinical stability of the implant.

In 1940, Bothe, Beaton, and Davenport, of Chicago, compared the tissue reactions using several different metals in an animal model (cats) in a continuing effort to expand upon the potential role electrolysis played in the surrounding tissue reaction. Using implants of dissimilar metals surgically placed into the same bone (cat femur), they demonstrated electrical potentials between the implants at 7 months. The following metals were used: cadmium, manganese, aluminum, tin, lead, titanium, copper, stainless steel, and vitallium. Their findings revealed, however, that the electrical potentials, while measurable after 7 months, were not closely correlated with the adjacent tissue reaction. Under their experimental conditions, where electrolytic action should have been favored by adjacent dissimilar metals, each metal retained characteristic individuality of reaction.⁴⁶ It was the inclusion of the metal titanium in their research that proved to be of great significance years later. They noted prophetically that: “The response of bone to titanium was as good, if not better, than that to the noncorrosive alloys, in that there was more tendency for the bone to fuse with it...if metallurgical developments of the future make it possible to work it into suitable shapes, it has the strength and hardness necessary for proper support. More experimental work is needed to prove it equal or superior to the noncorrosive alloys as a prosthetic material.”⁴⁶

Finally in 1951, Gottlieb S. Leventhal of Philadelphia, strongly endorsed titanium as an ideal metal for use in fixation of bone fractures.⁴⁷ He suggested this metal because of its superior characteristics with regard to its tensile and yield strength, weight, resistance to corrosion, ability to be welded and forged, and because it could be machined like stainless steel. Leventhal described what years later Brånemark called “osseointegration” when he placed titanium screws in rat femurs. Leventhal stated: “At the end of 6 weeks, the screws were slightly tighter than when originally put in; at twelve weeks, the screws were more difficult to remove; and at the end of 16 weeks, the screws were so tight that in one specimen the femur was fractured when an attempt was made to remove the screw. Microscopic examinations of the bone structure revealed no reaction to the implants. The trabeculation appeared to be perfectly normal.”⁴⁷

In the mid-1950s, Brånemark, an orthopedic surgeon, used titanium to study blood flow in animal research projects. While conducting his research, he found again that the material became solidly embedded in bone. The titanium was almost impossible for him to remove, and he called this phenomenon “osseointegration.” He hypothesized that this material might be capable of withstanding occlusal forces, and he began studying the use of titanium for tooth replacements. The shift from vitallium to titanium happened in the era of Linkow’s blade implants. The first blade implant was still made out of vitallium; the later designs were all titanium. Brånemark’s major contribution toward implant dentistry is his thorough documentation of the long-term success of titanium in animal and human studies before publishing his data in 1969.⁴⁸ In 1977, he published guidelines on the successful use of endosseous implants, and, in 1981, his research group published a 15-year follow up of their implant cases. Since then, the use of titanium root-form implants has been considered the state-of-the-art therapy to replace missing teeth.^49,50

DESIGN AND LOADING

In 1939, a publication by Strock stated: “When a less active material was used, as iridoplatinum by Greenfield, the mechanics involved probably accounts for the lack of success.”⁴¹ In other words, the reason Greenfield’s hollow-basket implant did not remain in implant dentistry since 1913 was not the bioincompatibility of the material, it was the mechanical loading pattern that decreased Greenfield’s success and made the dental profession suspicious of its predictability. Greenfield appeared to be unaware of the mechanical loading principles and their significance for implant success, even though his technique did not involve loading them immediately. The understanding of forces associated with implant dentistry is a topic that has just recently been researched through methods such as finite element analysis and case reports that show bone loss caused by overload.^51,52 During the time of Greenfield, Strock, and Linkow, many of the failures might have been caused, not by the material or the surgical technique that was used, but by early loading or excessive mechanical stress. Greenfield’s design of a hollow-basket implant seems unfavorable, as it limits the amount of implant surface area in contact with bone. In addition, he fabricated long-span bridges from canine to molar on those implants. Today, that would be considered overloading.⁵¹

Brånemark published his landmark papers in a time when the majority of dental implant publications dealt with the subperiosteal implant. Aside from the morbidity of the insertion, the subperiosteal implant functioned. However, many failures occurred just a few years after placement, likely caused by unphysiologic stress. Brånemark’s mechanical approaches were far more conservative than that of many others before and after his research. In his original research paper (1969), he measured the stability of the anchorage and claimed it to be excellent.⁴⁸ Brånemark’s implant design at that time evolved from the shapes used in orthopedic surgery. He worked in conjunction with an American-trained engineer, Richard Skalak. The first implants that he placed in humans were polished and screw-type in design. Linkow’s “blade vent” implant was introduced at about the same time that Brånemark published his initial report.⁵³ Blade implants became very popular for almost two decades, and a very wide range of different implant shapes appeared. Some of these were screw-type in design. The majority of Linkow’s implants were one-piece, meaning that the implant and the abutment were one piece, and had to be immediately loaded. As previously mentioned, research on mechanical loading and associated implant failure was lacking in the 1960s and 1970s. Nevertheless, it can be speculated that, as Greenfield before him, the majority of Linkow’s blade implants might have survived long-term, if the loading protocol had been better understood. However, the importance of biomechanics was not understood, and the clinical phenomenon that was encountered around many of the blade implants was a periimplant radiolucency called fibro-osseous integration.

In 1969, the majority of implant surgeons believed that a fibro-osseous connection was superior to a firm bone-to-implant contact, as it was believed that the fibro-osseous interface had a “shock absorbing capacity” similar to the periodontal ligament around a natural tooth. At that time, advances in implant understanding were hampered by undeveloped histological methods. Beginning in 1976, Schroeder and colleagues became capable of developing proof with their extensive histological research.⁵⁴ They demonstrated that the pseudoligament that formed after early or excessive loading of an implant was not the perpendicular orientation of fibers that is found around a natural tooth. Thus, periimplant radiolucencies failed to show the presumed shock absorbing capacity, and their nature was termed fibro-osseous encapsulation, indicating a pathological rather than an anatomical variation. Because the failure of blade implants and their associated negative reputation most likely is not related to implant material nor implant design, it can be assumed that if appropriate surgical techniques, materials, and loading were to be used, the blade implant would still be a good solution for a patient with a knife-edge ridge. Research regarding overheating bone while placing implants, the importance of a rough surface, immediate loading, and implant overload evolved years after the blade-implant design disappeared. The advantage of the blade implant design is that it frequently allows implant placement without the need for bone augmentation. The most significant disadvantage of blade implants, however, is the need for a more invasive surgery to place the blade. The split-ridge procedure, developed in that era, is technique-sensitive and allows implants to be placed in narrow ridges. It is conceivable that blades could still be an appropriate solution today; however, the design lost most of its credibility during the many years that it was associated with fibro-osseous encapsulation. This is similar to what had happened to Greenfield several years previously.

It is interesting to note that many of the designs initiated by Schroeder and colleagues between 1974 and 1985 (since 1980 the International Team of Oral Implantology [ITI]) “consisted of a hollow-cylinder, one-piece implant.”⁵⁵ A review article on the development of the ITI® Dental Implant System states: “Other elementary considerations in similar type and designs were described by Greenfield (1913) and Benaim (1959). Greenfield reported satisfactory results with his patented iridoplatinum lattice implant—probably the first clinically applicable endosteal implant.”⁵⁶ This type of implant design was part of the first series of ITI implants developed by this company. Later the company changed the design from a hollow-cylinder to a screw-type implant modified with holes to allow enhanced bone anchorage. The main goals of the ITI, a team of experts from all over the world, were and still are to do extensive research on biomechanics, design of the implant superstructure, and implant surfaces.⁵⁶ The Straumann Group provided the technical research facilities for the ITI. Their ongoing investigations provided implant dentistry with many of the clinical principles, such as loading protocols, that are used today.

SURGICAL TECHNIQUE

One of the major goals of dental implant manufacturers in the past decade has been to simplify the use of implants and to create more practical and logical implant placement techniques. The stepwise use of increasing drill diameters starting from a round bur is not a new concept. Greenfield provided a detailed description of that technique in 1913.¹¹ He described a distinct and logical method of using a soft-tissue punch, a guide drill, a pilot drill, and a final drill. His guide trephines had depth markings similar to modern guide drills. Greenfield related the anatomy of the recipient site in width and height to the size of the implant, and suggested using wider diameter implants for molar teeth. Currently, dentists use this rediscovered concept when using implant manufacturers’ recommendations for wide body or platform implants on molar teeth. Greenfield downplayed the importance of splinting implants, and he suggested the use of postoperative radiographs to confirm adequate implant position. He specifically emphasized that the osteotomy should have a precise fit (no micromovement) for the hollow cylinder, allowing stability of the artificial root. Today, this concept is called “primary stability.” He states that in the initial healing time, “the implant will be held firmly until a sufficient deposit of bone cells has filled the spaces in the root frame. Thus the artificial root becomes solidly embedded in the jaw.”11 Histological methods were not available at that time, but Greenfield’s account could be considered an early description of osseointegration. The theory of osseointegration relies on the histological proof of bone-to-implant contact.⁵⁴ This method was not applicable in 1913, but at least the idea of the clinical importance of osseointegration appears to date back to Greenfield.

SURFACE

The last significant contribution in implant dentistry was surface roughness. The recognition of the importance of a roughened surface dates back to Schroeder, Sutter, and colleagues (later ITI). Their research was initiated in 1974 and continued to evolve into the ITI-bonefit-implant. The first bonefit-implant was marketed in 1979 and was named the ITI-Type-F implant. This hollow cylinder, one-piece implant had a titanium-plasma sprayed surface.⁵⁷

During that time frame, the ITI research team histologically examined the bone-to-implant interface of the fibroosseous integration and proved it to be less favorable than osseointegration.⁵⁴ In addition, the research team found that by using a roughened surface, the percentage of bone-to-implant contact could be significantly enhanced.^54-58 The roughened surface can be considered another major breakthrough in implant dentistry.59 Rough surfaces decrease the time required after placement before mechanical loading. Roughened surfaces are believed to increase biocompatibility, and some surfaces are claimed to be “osteoinductive.” Research on implant surfaces led ITI to change the surface from titanium-plasma sprayed (TPS®) to sand-blasted and acid-etched (SLA®).^56-59 The company that evolved through Brånemark’s implant system, Nobel Biocare USA, LLC (Yorba Linda, CA), added the TiUnite® roughened surface to their implants. The innovation of rough-surface implants has paved the way for immediate implant placement after extraction and immediate loading with or without function.

FUTURE

Implant surfaces probably have the greatest potential for enhancement in implant dentistry. By adding proteins on implant surfaces, the bone-to-implant contact may increase further, and healing and loading time may be shortened. In addition, the surfaces may be capable of withstanding bacterial or load challenges to prevent bone breakdown and lessen implant failure.

CONCLUSION

In 1913, E. J. Greenfield, a little-known pioneer of the endosseous metal implant, provided the dental profession with many of the basic concepts of the nascent field of implantology. These concepts served as the foundation upon which later clinicians successfully built and raised the standard of patient care. Greenfield’s innovative and seminal contributions deserve the appropriate recognition afforded to those members of the dental profession who have greatly enhanced the practice of dentistry and the ability to serve patients.

ABOUT THE AUTHORS

• Robert J. Rudy, DMD, is an Associate Clinical Professor and Director of Predoctoral Periodontology at Tufts University School of Dental Medicine in Boston, Massachusetts.
• Paul A. Levi, Jr, DMD, is an Associate Clinical Professor in the Department of Periodontology at Tufts University School of Dental Medicine in Boston, Massachusetts; President of the American Academy of Periodontology Foundation; and a Diplomate of the American Board of Periodontology.
• FredJ.Bonacci,DMD,isaDiplomateofthe American Board of Periodontology; Former Resident in the Department of Periodontology at Tufts University School of Dental Medicine in Boston, Massachusetts; and maintains a private practice in Periodontolgy and Dental Implants in Forty Fort, Pennsylvania.
• Arnold S. Weisgold, DDS, is an Adjunct Professor of Periodontics in the Department of Periodontics at the University of Pennsylvania School of DentalMedicineinPhiladelphia,Pennsylvania.
• Daniel Engler-Hamm, DMD, Dr. Med. Dent., MSc, is a Diplomate of the American Board of Periodontology; Former Resident, Department of Periodontology, Tufts University School of Dental Medicine, Boston, Massachusetts; and maintains a private practice limited to Periodontics and Implant Dentistry in Munich, Germany.

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