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Current perspectives in residual ridge remodeling and its clinical implications: A review

Leila Jahangiri, BDS, MMSc,a Hugh Devlin, BDS, PhD,b Kang Ting, DMD, DMSc,c and Ichiro Nishimura, DDS, DMSc, DMDd Harvard School of Dental Medicine, Boston, Mass.; University Dental Hospital of Manchester, Manchester, United Kingdom; and UCLA School of Dentistry, Los Angeles, Calif. Purpose. This article reviews the current understanding of the biology of tooth extraction wound healing and residual ridge remodeling. Methods. The review of the biology of tooth extraction wound healing involves a discussion of the different cells populating the tooth extraction wound, the matrix formation, and the control of the repair process in the short-term. Defects in socket matrix formation or cellular activity will lead to stalled healing. The review of residual ridge remodeling describes the long-term result of tooth extraction and formation of residual ridges, in which the quantity of bone tissue continuously decreases. This may suggest that any potential regulatory factors of residual ridge resorption should have an adverse effect either on the increased catabolic activity by osteoclasts or on the decreased anabolic activity by osteoblasts. Both short-term tooth extraction healing and long-term residual ridge remodeling processes are interdependent. Furthermore, any potential genetic and environmental regulatory factors can affect the quality and quantity of bone by altering the gene expression events taking place in bone cells. Results. The intent of this article was to review the current progress of biologic research on residual ridge remodeling and to relate the changes at molecular, cellular, and tissue levels. The understanding of residual ridge remodeling may provide a sound scientific basis for improved restorative and therapeutic treatments of the edentulous population. (J Prosthet Dent 1998;80:224-37.)

This review addressed the cellular and extracellular matrix component of alveolar bone regeneration. The cellular component is sensitively responding to the mechanical and biologic environments such as removable partial denture and osteoporosis. Uncovering these regulatory mechanisms may lead to a new therapeutic modality in maintaining and further regeneration of the residual ridge alveolar bone. The heterogeneous reaction by osteoblasts to a newly characterized extracellular matrix containing type II and type IX collagens has provided a puzzling but exciting result, which seems to postulate two independent remodeling processes that regulate cortical bone and trabecular bone separately. The proposed distinct remodeling processes may be directly applied to osseointegration phenomenon in which cortical and trabecular bones may provide different consequences.

Presented in part before the Academy of Prosthodontics, Tucson, Arizona, May 1995. This review was partly based on investigations supported by Procter & Gamble Fellowship Award (L. Jahangiri), British Diabetic Association (H. Devlin), and NIH grants, EY08219, and DE10870 (I. Nishimura). aInstructor of Restorative Dentistry (Prosthodontics), Harvard School of Dental Medicine. bSenior Lecturer in Restorative Dentistry, University Dental Hospital of Manchester, University of Manchester. cAssistant Professor of Orthodontics, UCLA School of Dentistry. dAssociate Professor Section of Advanced Prosthodontics, UCLA School of Dentistry and Director, Center for Reconstructive Biotechnology. 224 THE JOURNAL OF PROSTHETIC DENTISTRY

esidual ridge is a term used to describe the shape of the clinical alveolar ridge after healing of bone and soft tissues after tooth extractions. After tooth extraction, a cascade of inflammatory reactions is immediately activated, and the extraction socket is temporarily closed by the blood clotting. Epithelial tissue begins its proliferation and migration within the first week and the disrupted tissue integrity is quickly restored. Histologic evidence of active bone formation in the bottom of the socket is seen as early as 2 weeks after the extraction and the socket is progressively filled with newly formed bone in about 6 months.1,2 The most striking feature of the extraction wound healing is that even


and 3 months (B). but the sequence of biologic events is not well-understood.JAHANGIRI ET AL THE JOURNAL OF PROSTHETIC DENTISTRY Fig. The size of the residual ridge is reduced most rapidly in the first 6 months.11 The rate of RRR is different among persons. which rely greatly on the quantity and architecture of the jaw bones. but the bone resorption activity of residual ridge continues throughout life at a slower rate. 1. • Rate is variable –between different persons –within the same person at different times –within the same person at different sites • Has a multifactorial cause –anatomic factor –prosthetic factor –metabolic and systemic factor –functional factor 225 . and even at different sites in the same person. 17 years (D). • The rate is fastest in the first 6 months after extraction.12-17 The RRR phenomenon is easily observed clinically after tooth extraction. progressive and irreversible. largely due to bone loss after tooth extraction. after the healing of wounds. Clinical features of reduction of residual ridges (RRR) • Definition Continuous size reduction of the residual ridge. 1). the residual ridge alveolar bone undergoes a life-long catabolic remodeling. Since the first reports of substantial resorption of the edentulous residual ridge by AUGUST 1998 Table I. Longitudinal observations by standardized lateral cephalographs on continuous resorption of maxillary and mandibular residual ridge before tooth extraction (A).3-10 This unique phenomenon has been described as residual ridge reduction (RRR) (Table I). Residual ridge remodeling directly affects the function of removable prostheses. Superimposed cephalographs depict that large amount of bone structure was removed during this time (F). resulting in removal of a large amount of jaw structure (Fig. 7 months (C). and 25 years (E) after extraction. • General feature RRR is chronic.

metabolic.32 Atwood and Coy31 Mercier and Inoue75 Kribbs et al. no single factor alone has been found to contribute to VOLUME 80 NUMBER 2 .122 Prosthodontic factor Immediate denture Decreased RRR No correlation Increased RRR Zero degree teeth Metabolic and systemic factor Age and sex No correlation with the rate of RRR Osteoporosis No correlation with the ridge height Ca and Vit D supplement Zinc sulfate supplement Dichloromethane diphosphonate supplement Sodium fluoride supplement Indomethacin supplement Functional factor Intensive denture wearing Smaller maxillary ridge Knife-edge type mandible Knife-edge type in monkeys Decreased RRR Better ext.115 von Wowern and Kellerup37 Nishimura et al.43 Carlsson et al. The primary goal of those descriptive studies was therefore to elucidate a pathologic cause of the severe form of RRR.119 Bergman and Carlsson120 Atwood and Coy31 van der Kuij et al.21-35 panoramic radiographs. prosthetic. These observations in edentulous patients are not conclusive and.29 Kelly47 Tallgren24 Nicol et al.40 Michael and Barsoum45 Wictorin25 Wictorin25 Johnson42.36.26-28 Carlsson et al.18 Atwood. Etiologic factors of reduction of residual ridges (RRR) Etiologic factor Correlation with RRR Source Anatomic factor Mandible Short and square face Large alveolar process Density of alveolar bone Labial alveoloplasty 4 × more RRR than maxilla Inconclusive Increased RRR Direct effect of masticatory force? Increased RRR No correlation with the jaw size Classification postulated No correlation with bone density Increased RRR No correlation Tallgren23 Atwood and Coy31 Tallgren23 Mercier and Lafontant113 Wictorin25 Atwood and Coy31 Wilson114 Atwood and Coy31 Gazabatt et al.THE JOURNAL OF PROSTHETIC DENTISTRY JAHANGIRI ET AL Table II. Atwood46 postulated that there are four major etiologic 226 factors that cause RRR: anatomic.35 Nishimura et al.32 Woelfel et al.76 Ortman et al. and functional factors. healing in hamsters Decreased RRR in rats No correlation (but better calcification) Decreased RRR in rats Increased RRR Regular denture wearing “Combination syndrome” No correlation with the rate of RRR (Statistically insignificant trend) Other factor Bioelectric potential Decreased RRR by exogenous pulsed electromagnetic fields in dogs Thompson.20 a number of studies have been conducted to describe the structure of the changing residual ridge using standardized measurements of lateral cephalographs.19 and Tallgren.33 Wictorin25 Carlsson26-28 Atwood and Coy31 Winter et al.37 or diagnostic casts.38-45 In 1979.63 Campbell38 Carlsson41 Carlsson et al. to date.121 Ortman et al.79 Wical and Brussee36 Mesrobian and Shklar116 Olson and Hagen117 Fenton and El-Kassem118 Nishimura et al.26-28 Winter et al.

LOCAL AND SYSTEMIC FACTORS INFLUENCING THE RESIDUAL RIDGE REMODELING Mechanical stress by prosthesis affecting bone resorption It is observed that patients with combination syndrome. However. Other studies pointed out that postmenopausal osteoporosis has attracted much attention in causal relation to RRR. Defects in socket matrix formation or cellular activity will lead to stalled healing. Panoramic radiograph (A) and intraoral photograph (B) of patients exhibiting severe localized bone resorption at anterior segment of maxillary residual ridge. The second objective was to review the current understanding of the biology of extraction wound healing. Hypothetical scheme (C) has been postulated that mechanical stress may induce local synthesis of messenger signals such as prostaglandins. cellular. Therefore this article reviewed current progress of biologic research on residual ridge remodeling. Thus. the list in Table II should serve only as an index for RRR studies. matrix formation. which then activate osteoclastic bone resorption (OC) at surface of residual ridge alveolar bone. and any potential genetic and environmental regulatory factors can affect the quality and quantity of bone by altering the gene expression events. The first objective of this article was to review local mechanical stress and systemic osteoporosis as potential factors that influence the long-term sequelae of tooth extraction and resorption of residual ridges. An exaggerated mechanical stress applied to the maxillary complete denture from the remaining mandibular anterior teeth has been postulated to cause this site specific RRR. It was suspected that excessive mechanical stresses were responsible for the less advantageous residual ridges observed in the institutionalized patients who wore their complete dentures for long hours than the edentulous ridges of the patients in the same institution who refused to wear their dentures. 2). Bar = 200 µm. The results from most of these studies are summarized in Table II.JAHANGIRI ET AL THE JOURNAL OF PROSTHETIC DENTISTRY Fig. either on the increased catabolic activity by osteoclasts or on the decreased anabolic activity by osteoblasts. 2. the severe form of RRR (Table II). it was not our intent to verify the data and conclusions of all these studies. which involves a discussion of the different cells populating the extraction site. and tissue levels. relating the changes at molecular.38 227 . The residual ridge is primarily composed of unique oral soft tissue and alveolar bone. and short-term control of the repair process. as described by Kelly. both of which are formed as a result of tooth extraction wound healing. although in-depth analyses are provided for the biologic data on tooth extraction socket healing and long-term residual ridge remodeling from selected articles. in which bone tissue is adversely affected.47 exhibit severe RRR in the anterior segment of maxillary residual ridge (Fig. however. all efforts were made to comprehensively list the dental literature that is thought to be relevant to RRR. there are several consistent observations that suggest that local mechanical stress often generated by removable prostheses may affect the state of residual ridges. AUGUST 1998 In this article.

(2) partial denture with bilateral free-end denture bases.58-60 Prostaglandins are a group of fatty acid derivatives synthesized by many different cells under stress and exert various biologic actions in the neighboring tissues.9. dental radiographs might be used to screen for systemic osteoporosis as there is much evidence that the mandible reflects the quantity of bone elsewhere in the skeleton. which appears to primarily bear the mechanical stress. The habitual chewing side of the facial bone. Mountain gorillas tend to use only one side of the jaw consistently until the teeth are totally worn so that food is no longer effectively held.69 Densitometry of the mandible. The possible involvement of prostaglandin in residual ridge remodeling has been suggested. Numerous radiographs are taken in general dental practice for the screening and diagnosis of conditions not relevant to osteoporosis. Type II osteoporosis reflects a composite of age-related changes in intestinal. When the bone tissue is placed in a state of immobilization or a weightless environment. Yeh and Rodan61 228 reported that repetitive mechanical stresses applied to osteoblastic cells in vitro significantly increased the prostaglandin E2 synthesis. and hormonal function.65.62 Because the systemic delivery of prostaglandin E2 successfully reverted the inhibitory effect of indomethacin. it bears less mechanical stress and cannot sustain the normal coupled remodeling process and results in loss of calcified bone mass described as disuse atrophy.71 and dual energy x-ray absorptiometry (DXA)72 all demonstrated significant relationships between systemic and mandibular osteopenia. and any other functional jaw movements.54 However. the edentulous mucosa shows remarkable tolerance. However. 2). the daily administration of indomethacin.6. In a separate study that used edentulous rats. Bone that receives constant mechanical stimuli maintain a coupled cellular activity between osteoclasts and osteoblasts. Both cortical and trabecular bone are affected in Type II osteoporosis. applied mechanical force can stimulate bone apposition.52. renal.68 A general radiolucency of the mandible might also be expected in those patients with systemic osteoporosis.63 For example.63 It is conceivable that biologic molecules locally synthesized in the edentulous mucosa may induce the osteoclastic activity on the surface of residual ridge alveolar bone (Fig. However. and hence to VOLUME 80 NUMBER 2 . one of clinical manifestations of “osteoporosis” is observed as less radiographic bone density. In either case.50 During mastication. particularly at the facial muscle attachment site.5. reduced the rate of RRR to 50% within the experimental period. exhibits a significant bone apposition to the extent that facial structure is often altered. The synthesis of prostaglandins in periodontal tissues has been postulated to play the “messenger” role in linking the mechanical stimulus to the osteoclastic activity.5. swallowing.62 The direct relationship between mechanical stress and residual ridge and prostaglandin-mediated bone resorption causing severe form of RRR has not yet been fully elucidated.48. the dentist might suspect osteoporosis in a person with a thinned mandibular cortex. and (3) partial denture with anterior alveolar bar. Relationships have been found in cadaveric bone samples between the specific gravity of edentulous mandible slices and the radius. notably in the trabecular bone. and no substantial inflammatory reaction is observed. and characteristically presents the bone mass loss. For example. The longitudinal observation of the edentulous ridge of these patients revealed the increased rate of RRR in the groups of wearing dentures.THE JOURNAL OF PROSTHETIC DENTISTRY JAHANGIRI ET AL A prospective clinical study addressing the mechanical factors on RRR was conducted by Carlsson et al. which is transmitted through the denture base and to the residual ridge. an inhibitor of cyclooxygenase (an enzyme required for the prostaglandin synthesis).4. The degree of residual ridge resorption is closely related to the time since tooth extraction. masticatory muscles produce force on the occlusal surface of artificial teeth. in the patient’s mouth.10.70 dual photon absorptiometry. Sharry et al. facial bone remodeling in mountain gorillas appears to closely correlate with their unique chewing habits.55-57 The mechanical stimulus applied to dentoalveolar tissue in orthodontic treatment is known to induce local bone remodeling. This unique environment may differentiate RRR from the common disuse atrophy concept. including bone resorption.64 Type I osteoporosis is defined as the specific consequence of menopausal estrogen deprivation.29 in which partially edentulous patients (Kennedy class I) were divided into three experimental groups wearing (1) no mandibular denture.49 Conversely. the local synthesis of prostaglandins was postulated to mediate the residual ridge bone resorption activity.3.51 examined bone stress patterns in dry skulls and reported that stress resulting from dentures may be transmitted over a rather wide area. The keratinized edentulous mucosa can be deformed as a result of pressure from dentures15-17.53 and vascular alterations such as arteriosclerosis may result from long-term denture wear.67. dentures are seated on the residual ridge mucosa overlying the bone directly. Osteoporosis and residual ridge remodeling The clinical and pathophysiologic views of osteoporosis has been refined recently to the concept of Types I and II osteoporosis.66 The microradiographic and histologic examinations of cadaveric mandibular bone samples from an elderly sample of edentulous persons have demonstrated that the mandibular bone undergoes considerable remodeling.

123 the age of the patient. bone resorption can result in changes of three-dimensional bone structure. and B) has been reported to associate with residual ridge mucosa with characteristic undercut (C. Postmenopausal women with lower bone densitometric scores exhibited a tendency to develop a knife-edge ridge in the mandible. the rate of residual ridge resorption has not been clearly shown to directly correlate with the bone density measured in the body of mandible and metacarpal bone.31.37 A knife-edged ridge is formed when bone resorption occurs at the labial and lingual surfaces of the residual ridge in preference to the occlusal surface. Because osteoclastic activity occurs on the surface of the residual ridge. arrow). 3. a combination of a small maxillary ridge and a knife-edge 229 . Combination of disadvantaged residual ridges (small maxillary residual ridge [Mx] and knife-edge mandibular residual ridge [Md]) is often presented in postmenopausal osteoporotic patients (A).74-76 These studies used the height of the mandibular edentulous ridge as the measurement of residual ridge resorption.JAHANGIRI ET AL THE JOURNAL OF PROSTHETIC DENTISTRY Fig.73 However. Knife-edge residual alveolar bone (A: Boxed.35 These results suggested that clinically less advantageous residual ridge conditions. The maxillary residual ridge was reported to be significantly smaller in AUGUST 1998 postmenopausal osteoporotic women while their edentulous mandible remained the same as the age-matched controls.

The radial arrangement of the developing bone trabeculae observed in their defects resembled the radial trabecular pattern observed on radiographs of healing tooth sockets. Trabeculae were absent where this preliminary collagenous framework failed to form. Recently. the initial ectomesenchymal cells directly differentiate into osteoblasts. whereas the osteoclastic bone resorption takes place on the surface of the residual ridge. Endochondral ossification is commonly seen at the growth plate of long bone. there is a tendency to form a knife-edge mandibular ridge as seen in postmenopausal women. Subsequent remodeling of the small primary trabeculae produced secondary trabeculae that resembled the original cancellous bone pattern.83 Because the residual ridge is composed of both cortical and trabecular bones. In addition to this immunologic phenotype. the major emphasis of current biologic studies of residual ridge remodeling is directed toward the characterization of this “template” stage of bone remodeling. Chondrocytes undergo sequential histodifferentiation. A two-stage process of bone formation is evident in endochondral ossification. However. which led to widespread effects on the immune system. osteoblasts can directly deposit osteoid tissue. the Senesent Accelerated Mouse (SAM) strain also presents “senile” osteoporotic bone features. This unique feature has been described by a general hypothesis that the tissue regeneration is considered to be a reiterated process of tissue embryogenesis.78 In ovariectomized monkeys. Hsieh et al. which is different from endochondral ossification. including tooth bearing alveolar process.84 Separately developed mutant mice.77. AND FORMATION OF THE RESIDUAL RIDGE A specific feature of residual ridge formation is that its essential components are formed as the consequence to healing of a significant bony and mucosal wound created by tooth extraction.93 bypassing the deposition and resorption of hypertrophic cartilage matrix.79 The detailed bone remodeling in the residual ridge was examined in ovariectomized rats. a combination of which results in a distinct porosity on the crest of the residual ridge alveolar bone (Fig. As demonstrated in a recent study. in which cartilage tissue is initially present. this unique surface tissue may be influenced by the systemic estrogen level and exhibit different remodeling patterns. synchondrosis of the skull base. The causal relationship between Type II osteoporosis and RRR has not been addressed. is formed through intramembranous bone formation. By using a bone vital staining method. maxillofacial bones. because of its potentials in guiding bone wound healing. One of the most obvious features of the healing of tooth extraction sockets is the absence of precursor cartilaginous tissue. The remnant hypertrophic cartilage matrix is believed to provide the template scaffold for osteoblasts to precipitate bone extracellular matrix. In intramembranous bone formation examined in calvaria. birefringent collagen fibers formed a preliminary framework along which the trabeculae were oriented and were fabricated by fibroblasts. and the defect in diabetes mellitus may be due to a reduced collagen production and an absence of these fibers. may be more prevalent in those patients with postmenopausal osteoporosis (Fig. marrow reticular cells. which is then calcified. 3). The delayed tooth socket healing often observed in poorly controlled diabetes inevitably causes a poor alveolar ridge contour. and mandibular condyle.85. VOLUME 80 NUMBER 2 TOOTH EXTRACTION. a line of transgenic mice was developed for the purpose of overproducing interleukin 4 (LCK-IL4 mice). the systemic condition of Type I osteoporosis may contribute to the different remodeling rates for the cortical bone and trabecular bone. characteristic bone disease involving both cortical bone and trabecular bone was observed. regeneration in the sheep after localized ablation. 87-89 Trabecular bone formation reaches the edge of extraction socket. 4).81 observed a significant increase in bone turnover and formation of immature woven bone in a trabecular area. and it has been hypothesized that this matrix serves as a template or framework that orientates the forming bone trabeculae. A dense network of collagen fibers normally fills the socket soon after tooth extraction. and osteoblasts. which result in cellular hypertrophy and apoptosis. WOUND HEALING. This uncoordinated remodeling pattern may result in the unique RRR pattern observed in postmenopausal female patients. Coarse.92 Precursor “template” collagens for bone wound healing The collagenous extraction socket matrix forms before bone formation.THE JOURNAL OF PROSTHETIC DENTISTRY JAHANGIRI ET AL mandibular ridge. Controversy surrounds the nature of the collagen molecules that provide this template function.90 Aaron and Skerry91 described trabecular bone 230 .80. In embryos. Li and Nishimura82 reported a unique surface structure of the residual ridge alveolar bone depicted in scanning electron micrographs associated with ovariectomy pretreatment.86 The previously mentioned mouse models have great potential to be used for human Type II osteoporosis studies and may provide a long-awaited opportunity to investigate the effect of “senile” osteoporosis on residual ridge remodeling. Ovariectomized animals have been intensively characterized and used in many studies as a model for human Type I osteoporosis. Histologic studies of residual ridges indicate that extraction sockets heal with active synthesis of trabecular bone. The template cartilage matrix is eventually resorbed.

unrelated to chondrogenesis. E.94-96 Type II collagen is a major collagen type of hyaline cartilage and thus has been long considered to contribute to the structural integrity of cartilage tissue and provide a template during endochonAUGUST 1998 dral ossification.JAHANGIRI ET AL THE JOURNAL OF PROSTHETIC DENTISTRY Fig. B. type II collagen has been further investigated and its two alternative splicing variants of type IIA and type IIB are found to have differing cell 231 . It is of particular interest that recent investigations reported the transient expression of cartilaginous procollagen type II mRNA during intramembranous bone formation.97 In recent years. 1 week after extraction of mandibular central and lateral incisors. bar = 50 µm). Occlusal radiographic observations of extraction socket healing in monkey suggest that active trabecular bone formation takes place at bottom of socket. C. The involvement of type II procollagen mRNA in different tissues other than cartilage may suggest some as yet undefined function of type II collagen. 12 weeks). 4. D. 3 weeks. 6 weeks. Goldner’s trichrome staining. Histology of cadaveric mandibular specimen depicting porosity at top of residual ridge alveolar bone resulted from unique bone wound healing in socket mostly with trabecular bone formation (F. 9 weeks. while cortical bone is subjected to bone resorption (A.

origins. Because of the exposed perifibril location and the interactive peptide structure of type IX collagen.101 Analysis of studies on the uncomplicated healing of extraction wounds have shown that after the clot formation. exons 2 and 3 are alternatively spliced. The surface of this fibril is associated with small collagen type IX.101 A puzzling finding is that investigators have failed to detect the presence of protein collagen type II by way of immunohistochemical studies in actively healing extraction sockets. it has been postulated that combination of type IIA and short type IX collagens may be synthesized. A cluster of cells that are associated with the early socket wound healing have been shown to express type II collagen mRNA.89. which misses NC4. During alveolar bone wound healing. granulation tissue is gradually replaced by connective tissues and later by intramembranous bone. Cartilage tissue predominantly synthesizes combination of type IIB and long type IX collagens.99 Type IIA is found in noncartilaginous tissues. Some of the questions that need to be answered include: Which splicing variant of type II collagen is expressed in the extraction socket? What are the role of these cells in the socket healing if type II collagen protein is synthesized? Do systemic or local factors influence the gene expression pattern during socket healing? Two-stage process of bone formation Cartilage collagen fibrils are composed of a group of different types of collagens including type II. whereas activation of downstream promoter generates short form type IX collagen. Type IIA and IIB collagen isoforms are synthesized as result. 5). it has been postulated that type IX collagen plays a molecular bridging role in the extracellular matrix and contributes to formation of a cartilage tissue architecture. without cartilage formation.89 VOLUME 80 NUMBER 2 . In type IX collagen gene. Diagram of alternative expression of α1(II) collagen and α1(IX) collagen genes generating tissue specific forms of collagen molecules. 5.THE JOURNAL OF PROSTHETIC DENTISTRY JAHANGIRI ET AL Fig. In type II collagen gene.101 This may be suggestive of either lack of collagen type II translation or difficulties in 232 detecting this protein in the healing socket.98. Use of upstream promoter results in synthesis of long form type IX collagen containing amino-terminal NC4 globule. two separate promoter/transcriptional start sites are found.100 The expression of type II procollagen mRNA has been identified in the healing extraction sockets in experimental animals by the method of RNA transfer blot analysis and in situ hybridization.102 It has been reported that collagen type IX mRNA is also expressed in early healing stages of extraction sockets.89. These alternative gene expression mechanisms appear to be used in tissue specific fashion. whereas type IIB has a strong association with chondrocytes and cartilage tissue formation (Fig.

Because type II collagen comprises the major constituent of cartilage. which was expressed in the extraction socket. Further analyses of residual ridge remodeling in rats have revealed that the α1(IX) collagen mRNA. 5). In many situations. Thus.JAHANGIRI ET AL THE JOURNAL OF PROSTHETIC DENTISTRY Fig.106 in which the principle orthogonal fiber architecture of the mature cornea is organized according to the template tissue. Such transgenic animals can provide a powerful tool to investigate the consequences to the missing biologic role of a specific molecule.103 Therefore this alternative expression of the short form of type IX collagen. one can generate animals harboring an experimentally introduced mutation to the molecule or inactivate the corresponding gene (Fig.104 It has been characterized in the similar transient expression of the short form of type IX collagens along with type II collagen in embryonic chicken cornea. which provides next generation of transgenic mice for various evaluations. and a severe retardation of growth for practically all bones. due to existence of unaffected chromosome. The detailed molecular assembly of type II and the short AUGUST 1998 form of type IX collagen in bone remodeling is not elucidated. a cleft palate. Target gene that has been manipulated in vitro to introduce mutation is introduced into mouse embryonic stem cells. was different and markedly shorter than that of cartilage. However. a short snout. Transgenic and inactive gene allelic manipulation in experimental animals To understand the role of a specific molecule. as used in avian eye formation. Transgenic mice with functionally impaired type II collagen result in chondrodysplasia with dwarfism. 89 The short form of type IX collagen omits the multiple exons. However. F1 chimera population is established. 6. Several transgenic mice have been generated with defective type II collagen. homozygous mutant mice carrying mutation in both pairs of chromosomes are used to examine effect of introduced mutation by comparison with wild type litter mates. that encode the amino-terminal globular domain (Fig.109 The introduced mutated pro α1(II) collagen chain appears to be included in a procollagen molecule and prevents folding into a stable triple helix. Recent immunohistochemical data suggest that type IX collagen is present only in the early bone formation stages of extraction socket healing and seems to disappear during the maturation stages.105. Heterozygous mutant mice often exhibit a milder phenotype.108. short and thick limbs. the function of the short form of type IX collagen in residual ridge remodeling remains to be clarified. After introduced mutant gene is incorporated into mouse chromosomes. a cranial bulge. which lacks the interactive peptide structure. the principal con233 . 6). may explain why cartilage tissue is not assembled in the extraction socket.107 Both cornea and bone possess the similar orthogonal pattern of collagen fibrils. embryonic stem cells are implanted in pseudopregnant mothers. delayed mineralization of bone. it is tempting to speculate that the transient matrix containing short type IX collagen may be involved in a tissue guiding role in alveolar bone repair. Diagram of transgenic mouse generation. primary cornea stroma.

Some homozygous transgenic mice displayed mild proportionate dwarfism. including both promoters. otherwise. α1(IX) collagen knock-out transgenic mice were developed. onset of 234 osteoarthritic changes became apparent particularly in the anterior part of the weight bearing area of the tibia. bar = 20 µm). Different extraction socket wound healing found in wild type mouse (A. arrows). They reported that even before the histologic onset of osteoarthritis. These data suggest that there may be two distinct bone remodeling processes. and the end plates in the mid-dorsal region were irregular. The results indicated that the trabecular bone pattern was often disturbed in “knockout” mice with some formation of cortical bone within the socket. Wild type and homozygous mutant mice were analyzed to elucidate the role of type IX collagen in residual ridge remodeling. 7). After reaching maturity. 8. Recently. However.110 reported the generation of transgenic mice harboring the minigene of α1(IX) collagen with an inframe deletion of the central domain. the offspring of the transgenic mice survived to their maturity. the presence of type II and IX collagen VOLUME 80 NUMBER 2 . 7. Postulated bone remodeling processes that may regulate trabecular bone and cortical bone separately. (Hematoxylin and eosin staining. The vertebral bodies were ovoid in shape as a result of a mild ossification defect. it is interesting to note that both endochondral bones and intramembranous bones are affected by the type II collagen mutation. the specimens were obtained at 7 days and 14 days after tooth extraction. which may provide novel blueprint for trabecular bone pattern formation. type IX collagen “knock-out” mice showed loss of trabecular bone restoration pattern with relatively normal cortical bone at bottom of socket (B. The ophthalmopathy was found in about 15% of transgenic animals.THE JOURNAL OF PROSTHETIC DENTISTRY JAHANGIRI ET AL Fig.111 The Neo gene was inserted in the exon 8 of the α1(IX) gene by homologous recombination. including localized bone remodeling. The extraction socket of mice with inactivated α1 (IX) alleles indicated that there was a considerable retardation in the formation of the trabecular bone pattern as compared with the healing socket of the control genotypically normal mice (Fig. Furthermore. These results strongly indicate that type IX collagen may play diverse biologic roles in various tissues. In the trabecular bone remodeling. a significant decrease in the intrinsic compressive stiffness was found in the articular cartilage of the transgenic mice.112 To evaluate alveolar bone repair. Bone healing in transgenic mouse was characterized by loss of trabecular bone formation at bottom of extraction socket (A. Nakata et al. arrows). Therefore this animal model allows an investigation of the functional role of type IX collagen as a potent element for alveolar bone regeneration. bar = 50 µm) and type IX collagen null transgenic mouse (B. sequence of this mutation is anticipated to cause disorganization of the growth plate. corneas of the transgenic offspring appeared opaque or irregular and were sometimes infiltrated by capillary vessels. which resulted in the total inactivation of α1(IX) alleles.) Fig. However. Trabecular bone remodeling is hypothesized to be dependent on prior expression of type II and IX collagens.

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Shklar G. The binding is durable buckram with the journal name. Toman D.. Hay ED. The effect of dietary zinc sulfate supplements on the healing of experimental extraction wounds. 107. Fassler R. AUGUST 1998 237 . BIOMIMETICS AND HOSPITAL DENTISTRY UCLA SCHOOL OF DENTISTRY 10833 LE CONTE AVE.73:2277 [abstract]. Hagen A. Shipping charges are included. Olsen BR. Metsaranta M. Proc Natl Acad Sc USA 1988. St. Ono K. Nakata K. Proc Natl Acad Sci USA 1991. Rosati R. J Periodont Res 1982. Carlsson GE. Fenton AH. Mesrobian AZ. Karger. Vandenberg P. Muragaki Y.46:250-5. Proc Natl Acad Sci USA 1994.53:56-61.00 ($97. J Biol Chem 1988. and all advertising is removed. Skeletal osteopenia and residual ridge resorption. Cartilage type IX collagen-proteoglycan contains a large aminoterminal globular domain encoded by multiple exons. Ting K. Sillevis Smitt PA. Fitch JM. Wilson JH. Devl Biol 1988. Bergman B. 103. Reife RA.199:129-40. 113. or (314)453-4531.85: 7496-500. Bioelectric stimulation and residual ridge resorption. Some aspects of diagnosis and design. Partial denture construction. In: Monographs in developmental biology. 121. Schnegelsberg PN. Proc Natl Acad Sci USA 1993. Tissue specific form of type IX collagen-proteoglycan arise from the use of two widely separated promoters. Payment must accompany all orders. Dausman J. Mayne R.128:396-405. Patient response to variations in denture technique. 80 (July-December). J Dent Res 1984. (CHS) LOS ANGELES. Helminen H.88:7640-4. Sandell LJ. 10/1/87547 Bound volumes available to subscribers Bound volumes of The Journal of Prosthetic Dentistry are available to subscribers (only) for the 1998 issues from the publisher at a cost of $84. Inoue S. Hoyland J.41:368-72. Vol. Casey DM. New York: S.347-63. Atwood DA. Knife-edge residual ridges: a clinical report.00 international) for Vol. Proc Natl Acad Sci USA 1991. 112. Hausmann E. Unger JW. Mercier P. Freemont AJ.40:181-5. Ting K. 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Fine structure of the developing avian cornea. 122. Olsen BR. volume number. Acquisition of type IX collagen by the developing avian primary corneal stroma and vitreous. 0022-3913/98/$5. Vasios G. J Biol Chem 1989. 111. Olsen BR. Reduced amounts of cartilage collagen fibrils and growth plate anomalies in transgenic mice harboring a glycine-to-cycteine mutation in the mouse type II procollagen alpha 1-chain gene. Nishimura I. Immunohistologic localization of type IX collagen during intramembranous bone formation. AlaKokko L. Dent J Aust 1949. Sugrue SP. Linsenmayer TF. 119. Somes GW. Inhibition of post-extraction alveolar ridge resorption in rats by dichloromethane diphosphonate.JAHANGIRI ET AL THE JOURNAL OF PROSTHETIC DENTISTRY 100.67:61-71. 1. 105. Reducing residual ridge reduction. Mice lacking alpha 1(IX) collagen develop noninflammatory degenerative joint disease. Olsen BR. Louis. Vaughan J. de Groot K. Reconstr Surg Traumatol 1985. Alternative splice form of type II procollagen mRNA (IIA) is predominant in skeletal precursors and noncartilaginous tissues during early mouse development. Nishimura I. Ortman LF. Volumes 77 and 78 are also available. Each bound volume contains a subject and author index. Nanlin AM. Fuhrmann J. 120. J Dent Res 1994. Sloan P. Nishimura I. Prockop DJ. Bound volumes are not available in place of a regular Journal subscription. Osteoarthritis associated with mild chondrodysplasia in transgenic mice expressing alpha 1(IX) collagen chains with a central deletion. Embryonic chicken cornea and cartilage synthesize type IX collagen molecules with different amino-terminal domains.17:669-74. Nishimura I. Ortman LF. Ellinger CW. MO 63146-3318. Revel J-P. 118.264:20033-41. 101. J Prosthet Dent 1985. 116. Khillan JS. Localization of procollagen type II mRNA and collagen type II in the healing tooth socket of the rat. USA. 110. CA 90024-1668 Copyright © 1998 by The Editorial Council of The Journal of Prosthetic Dentistry. 123. 1969.19:98105. Deers M. 115. Konomi H. van der Kuij P. Ninomiya Y. Contact Mosby.91:5070-4. Mentzer A. Nicol BR.63:1427. van der Rest M. Garofalo S. Svoboda KK. J Prosthet Dent 1981. Arch Oral Biol 1995. Part II: five-year cephalometric evaluation. Dunford RG.263:2324-9. 117. 114. Olsen BR.74:1652 [abstract]. The effect of fluoride on post-extraction alveolar resorption in the rat. 11830 Westline Industrial Drive. Devlin H. Expression of a partially deleted gene of human type II procollagen (COL2A1) in transgenic mice produces a chondrodysplasia.