Bone Quality: A Reality for the Process of Osseointegration : Implant Dentistry

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Clinical Science and Technology

Bone Quality: A Reality for the Process of Osseointegration

Sakka, Salah DDS, MSc, PhD*; Coulthard, Paul BDS, MDS, PhD

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doi: 10.1097/ID.0b013e3181bb840d
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The well-accepted concept of osseointegration has undoubtedly been one of the most scientific breakthroughs in dentistry over the past years. It is a good indication of the clinical success of titanium implants referring to the direct anchorage of such implants to the surrounding host bone.1 The definition of osseointegration by Brånemark2 has primarily been focused on its clinical capacity. He defined it as “a direct structural and functional connection between ordered living bone and the surface of a load carrying implant. Creation and maintenance of osseointegration, therefore, depends on the understanding of the tissue's healing, repair, and remodeling capacities.” The quantity and quality of the bone available are highly associated with the type of surgical technique and the type of implant, and both of these factors play an essential role in the success of oral implant surgery.3 Clinical reports show that oral implants placed in the mandible have higher survival rates than those placed in the maxilla.4,5 Here, bone quality is considered to be the main cause of such difference in the survival rates between the 2 jaws and which the mandible has the superiority in this matter.6 The development of computed tomography (CT) has allowed for better evaluation of the proposed implant sites and provided diagnostic information for both the mandible and the maxilla.7–9 It also allows for the bone-to-implant interface to be illustrated in greater detail.10 The Hounsfield Units determined by the software programs in the CT machines refers to the density of structures within the image. Such density is quantitative and can be used to differentiate various tissues in the examined site and characterize bone quality.11–13 Moreover, the local bone density has an existing influence on primary stability, which is an important determinant for implant success.14 The importance of bone quality is well recognized by implantology clinicians but is difficult to measure scientifically. Both structural morphology and cellular characteristics are essentially considered when bone quality is classified in the field of implantology.

Structural Morphology

The most commonly quoted classification is that suggested by Lekholm and Zarb,15 which distinguishes 5 classes of jaw atrophy and 4 types of bone quality: almost the entire jaw is composed of homogenous cortical bone (type 1), a thick layer of cortical bone that surrounds a central part of dense trabecular bone (type 2), a thin layer of cortical bone that surrounds dense trabecular bone of favorable strength (type 3), and a thin layer of cortical bone that surrounds low density trabecular bone (type 4). On the other hand, 4 basic divisions of available bone for oral implants, which follow the natural resorption phenomena were documented.16 These 4 classes have been extended to offer a well-planned approach to implant treatment options for surgery and prosthodontics.17,18 Furthermore, a density index based on the classification by Lekholm and Zarb15 was presented by Misch19 with comprehensive guidelines, such as treatment planning, surgical approach, and duration of healing for the various bone situations. Nevertheless, the classification of Lekholm and Zarb15 forms a simplified representation as alveolar bone is extremely inconsistent in cross sections and the transitional stages of bone quality between anterior and posterior jaw-bone are apparent.20,21 Moreover, classification of bone is rather practical, depending on the skill of the surgeon that leads to a high distinction in classifying bone to the previously stated 4 qualities. In addition, bone quality can also be determined by CT scans,22 cutting torque,23 and resonance frequency assessment of implant stability24,25 that have a major role in the success of osseointegration.

According to the above-mentioned classification of bone quality,15 placing implants into type 1 to type 3 bone leads to good clinical outcomes whereas type 4 is linked with a lower success rate26 that is related to the lack of adequate provision of implant primary stability to attain successful osseointegration. Here, such stability of implants in type 4 bone can be increased by means of manual condensation of the bone around implants27 in addition to the application of implants that have rough surface. Studies show that smooth titanium surfaces have less percentage of bone implant contact when compared with rough titanium surfaces.28,29 Ingrowth of complete bone with vascular supply would need a pore of 100 μm.30 Furthermore, the importance of surface roughness on the micrometer scale was also investigated in several experimental studies.31–33 The results showed higher removal torques and higher percentages of bone-to-implant contact for implant blasted with 25- and 75-μm particles of aluminum oxide. Thus, a specific surface roughness on the endosseous section of the implant enhances the regeneration potential at the interface, thus improving clinical implant osseointegration.

In addition to the ratio between cortical and trabecular bone, the latter hold information with regard to bone quality. Trabecular bone is filled with bone marrow, the source of osteoblasts and osteoclasts, and has therefore a higher turnover than cortical bone.34 Histomorphometric studies also show that trabecular bone volume differs between sexes (M > F), maxilla and mandible (mandible > maxilla), and posterior and anterior alveolar bone (anterior > posterior).20,21 Moreover, 3 classes of trabeculation were recognized by assessing the mandibular trabecular pattern in periapical radiographs.35 However, although these observations might be used for planning, performance, and prognosis of implant treatment, it remains unidentified whether trabecular structures alone can predict successful osseointegration.

Studies also stress the importance of bone volume when planning for oral implants where at least 10 mm and 6 mm in height and 5 mm and 6 mm in width for the maxilla and the mandible, respectively, are required for successful placement.36,37

The structural aspect and the volume of the bony host site are both essential elements when defining bone quality. However, other cellular characteristics have to be considered.

Cellular Characteristics

The principles of bone regeneration that follow implant placement may refer to the potential cellular characteristics of bone quality. These may include fibrin-rich matrix and platelets, inflammatory cells, angiogenesis, mesenchymal progenitor cells, bone morphogenetic proteins (BMPs), and bone resorption (Table 1).

Table 1:
Cellular Characteristics of Bone Quality and Their Possible Contribution to the Process of Osseointegration

Bone healing is a great biological effort of the skeletal tissues in which regenerative process restores the original structure and function. This is performed by a sequence of cellular activities, which will be similar to the development of bone during embryonic and postnatal life.38 Stages of osseointegration can be compared with the similar process of fracture healing, in which fragments become united, without the interference of fibrous tissue. A basic difference, however, exists; osseointegration unites bone to an implant surface.

Three stages can be recognized during the progression of fracture healing: inflammatory, reparative, and remodeling.39 The inflammatory stage occurs when disturbance of the vascular contribution to the periosteum leads to hematoma and cell death. Disrupted blood vessels are filled with fibrin that grants a matrix in which activated platelets release the content of their granules40 that contain growth factors like platelet-derived growth factor and transforming growth factor-b. Platelets have also investigated for their role in enhancing bone regeneration.41,42 After platelets activation, neutrophils and monocytes/macrophages invade the blood clot and initiate its substitution by granulation tissue.40 Monocytes release inflammatory cytokines such as interleukin-1 and interleukin-6, and tumor necrosis factor-a that increase prostaglandin synthesis. Inhibition of prostaglandin synthesis impairs fracture healing and most likely the process of osseointegration.43,44 At this point, successful osseointegration of oral implants might be linked to monocytes/macrophages and prostaglandins synthesis. Monocytes/macrophages also release the central mediators of angiogenesis such as vascular endothelial growth factor and basic fibroblast growth factor.45 Here, new capillaries are generated from already existing vasculature offering nutrients and oxygen to new developing tissue of woven bone.46 Studies confirm the formation of microvessels between oral implants and the hosted bone.47,48 Hence, the low success rate of osseointegration could be caused by impaired angiogenesis due to the interruption of blood vessels formation when implant stability is not achieved. Primitive mesenchymal progenitor elements would be chemotactically attracted by the necrotic tissue and would differentiate into mature cellular elements such as osteoblasts that subsequently produce type III collagen and chondrocytes that produce type II collagen indicative of the reparative stage.49 The differentiation potential of mesenchymal progenitor cells can serve as a characteristic of bone quality. This differentiation is controlled by local factors such as oxygen tension and BMPs.50 The latter are highly expressed at sites of bone repair51 and surface treatment of implants with recombinant BMPs can enhance osseointegration52 that may refer to their role in that pivotal process. On the other hand, high oxygen tension leads to an osteogenic phenotype whereas hypoxia favors the growth of chondrocytes.50 Angiogenesis is, therefore, an essential requirement for osteogenic differentiation of mesenchymal progenitor cells.

The bone remodeling stage begins with osteoclastic resorption to replace the existing woven bone by mature lamellar bone. Despite the fact that osteoclasts are responsible for excessive bone resorption and implant loss during chronic inflammation,53 their activity is essentially required after implant placement to resorb damaged bone.54 This would suggest that the osteoclastic activity can contribute to the process of osseointegration and may therefore be considered as one characteristic of bone quality.


The ratio between cortical and trabecular bone in addition to bone volume and density have a prevailing influence on implant success. Cellular characteristics of bone quality including monocytes/macrophages, mesenchymal progenitor cells, fibroblasts, osteoclasts, and cells associated with angiogenesis may contribute to the success of the local process of osseointegration. Also, local factors prostaglandins and BMPs play a role in regulating the function of cells involved in bone regeneration. However, how to determine the potential cellular characteristics of bone quality in different areas remain an unsolved question. Therefore, more studies are indicated to prove the prognostic value of such characteristics and to precisely conclude their part as useful predictors of successful osseointegration.


The authors claim to have no financial interest in any company or any of the products listed in this article.


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Abstract Translations


AUTOR(EN): Salah Sakka, DDS, MSc, PhD, Paul Coulthard, BDS, MDS, PhD.

Qualität des Knochengewebes: Eine Realität im Prozess der Knochengewebsintegration

ZUSAMMENFASSUNG: Die vorliegende Arbeit wirkt unterstützend in Richtung auf die Bedeutung des ursprünglichen Zustands der Knochengewebsqualität sowie deren ultimative Auswirkung auf den Erfolg einer Zahnimplantierungsbehandlung. Eine hohe Erfolgsquote für den Erhalt des alveolären Knochengewebes im Bereich um Zahnimplantate herum is bedingt durch eine gute Knochengewebsqualität. Für Implantologen sollte daher die Klassifizierung der Knochengewebsqualität auf den für die Knochengewebsintegration erforderlichen Schlüsselelementen aufbauen. Dazu gehören die strukturelle Morphologie sowie die zellulären Eigenschaften, wie Monozyten/Makrophagen, mesenchymale Stammzellen, Fibroblasten, Osteoklasten und Zellen, die mit dem Gefäßwachstum in Verbindung gebracht werden.

SCHLÜSSELWöRTER: Knochengewebsqualität, Knochengewebsintegration, orale Implantate, Knochenheilung


AUTOR(ES): Salah Sakka, DDS, MSc, PhD, Paul Coulthard BDS, MDS, PhD.

La calidad del hueso: una realidad para el proceso de integración ósea

ABSTRACTO: Este trabajo describe la condición inicial de la calidad del hueso y su efecto final en el éxito del tratamiento con implantes dentales. Una alta tasa de éxito para la preservación del hueso alveolar alrededor de los implantes dentales se calcula según la buena calidad del hueso. Para los implantólogos, la clasificación de la calidad del hueso debería basarse en los elementos claves requeridos para la integración ósea. Los mismos incluyen la morfología estructural y las características celulares tales como monocitos/macrófagos, células madre mesenquimales, fibroblastos, osteoclastos y células asociadas con la angiogénesis.

PALABRAS CLAVES: calidad del hueso, integración ósea, implantes orales, curación del hueso


AUTOR(ES): Salah Sakka, Cirurgião-Dentista, Mestre em Ciência, PhD, Paul Coulthard Bacharel em Odontologia, Mestre em Cirurgia Dentária, PhD.

Qualidade do Osso: uma Realidade para o Processo de Osseointegração

RESUMO: Este artigo contribuiu com a condição inicial de qualidade do osso e seu efeito definitivo sobre o sucesso do tratamento de implante dentário. Uma alta taxa de sucesso para a preservação do osso alveolar em torno de implantes orais pressupõe boa qualidade do osso. Para os implantologistas, a classificação da qualidade do osso deveria se basear nos elementos-chave exigidos para a osseointegração. Esses incluem a morfologia estrutural e características celulares como monócitos/macrófagos, células progenitoras mesenquimais, fibroblastos, osteoblastos e células associadas com a angiogênese.

PALAVRAS-CHAVE: qualidade do osso, osseointegração, implantes orais, cura do osso



АВТОРЫ: Salah Sakka, доктор xирургичE=ской стоматологии, магистр E=стE=ствE=нныx наук в области мE=диЦины, доктор философии, Paul Coulthard, бакалавр xирургичE=ской стоматологии, магистр xирургичE=ской стоматологии, доктор философии

КачE=ство кости: сущность проЦE=сса остE=оинтE=граЦии

РEЗЮМE: В данной статьE= приводятся доводы в поддE=ржку исxодного состояния качE=ства кости и E=го итогового воздE=йствия на успE=x лE=чE=ния с использованиE=м зубного имплантата. Высокая стE=пE=нь успE=шности для соxранE=ния альвE=олярной кости вокруг имплантатов, устанавливаE=мыx в ротовой полости, прогнозируE=тся при xорошE=м качE=ствE= кости. КлассификаЦия качE=ства кости для имплантологов должна основываться на ключE=выx элE=мE=нтаx, нE=обxодимыx для остE=оинтE=граЦии. Эти элE=мE=нты включают в сE=бя структурную морфологию и xарактE=ристики клE=точного строE=ния, такиE= как содE=ржаниE= моноЦитов / макрофагов, клE=ток-прE=дшE=ствE=нников в мE=зE=нxимE=, фибробластов, остE=окластоЦитов и клE=ток, связанныx с ангиогE=нE=зом.

КЛЮХEВЫE СЛОВА: качE=ство кости, остE=оинтE=граЦия, имплантаты в ротовой полости, заживлE=ниE= кости


YAZARLAR: Salah Sakka, DDS, MSc, PhD, Paul Coulthard, BDS, MDS, PhD.

Kemik Kalitesi: Osseoentegrasyon Sürecinin bir Realitesi

öZET: Bu çalışma, kemik kalitesinin ilk durumunu ve bunun dental implant tedavisinin nihai başarısı üzerine etkisini savunmaktadır. Oral implantların etrafındaki alveoler kemiğin korunmasında büyük başarı elde edilmesi, iyi kemik kalitesine bağlıdır. İmplantoloji uzmanları, kemik kalitesini osseoentegrasyon için gerekli anahtar unsurlara dayanarak sınıflamalıdırlar. Bunlar arasında yapısal morfoloji ve monositler/makrofajlar, mezenkimal projenitör hücreleri, fibroblastlar, osteoklastlar ve anjiyogenez ile ilgili hücreler gibi hücresel özellikler yer almaktadır.

ANAHTAR KELİMELER: kemik kalitesi, osseoentegrasyon, oral implantlar, kemik iyileşmesi







bone quality; osseointegration; oral implants; bone healing

© 2009 Lippincott Williams & Wilkins, Inc.