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 Table of Contents  
REVIEW ARTICLE
Year : 2012  |  Volume : 8  |  Issue : 6  |  Page : 85-93

Dental implants in irradiated jaws: A literature review


Department of Dental and Prosthetics Surgery, Tata Memorial Hospital, Mumbai, India

Date of Web Publication24-Jan-2012

Correspondence Address:
Kanchan P Dholam
Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Mumbai
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.92220

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 > Abstract 

Surgical treatment of head and neck cancer frequently results in defects that challenge conventional prosthetic rehabilitation. Successful rehabilitation using tissue supported dentures in such cases has been reported to be less than 20%. With the loss of jaw bones and thus the support, there is loss of retention to a great deal. Also, teeth loss on the side of the defect adds to failure in retention. Scar tissue formation, deviation of jaw due to muscle pull, decreased mouth opening, loss of sulcus and non vertical force are some of the common adversaries of jaw resection especially mandibular resection which pose great limitation on the stability and success of prospective prosthetic rehabilitation.
The advent and application of biologically acceptable implants in clinical dentistry has contributed to restoring the defects of the deficient maxillofacial systems. Surgical intervention in patients who had received head and neck irradiation is preferably avoided as it has been associated with decreased healing and increased potential for development of osteoradionecrosis. Hence an implant as an option when surgical field has received tumerocidal radiation is empirically excluded.
The purpose of this article is to review the studies and reports published in various journals related to osseointegrated implant rehabilitation in irradiated bones.

Keywords: Dental implants, osseointegration, radiation


How to cite this article:
Dholam KP, Gurav SV. Dental implants in irradiated jaws: A literature review. J Can Res Ther 2012;8, Suppl S2:85-93

How to cite this URL:
Dholam KP, Gurav SV. Dental implants in irradiated jaws: A literature review. J Can Res Ther [serial online] 2012 [cited 2019 Dec 15];8:85-93. Available from: http://www.cancerjournal.net/text.asp?2012/8/6/85/92220


 > Introduction Top


Rehabilitation following resection and reconstruction in head and neck cancer patients is a challenging goal to achieve. Adversaries of jaw resection limit the success of prospective rehabilitation. Today the defect of the deficient maxillofacial system can be restored with prosthesis anchored on to dental implants.

The search for cure of head and neck malignancies by surgery or medicine has its own disadvantage. Radiotherapy in head and neck regions lead to radiation caries. The replacement by conventional means of fixed prosthodontics is contraindicated in high caries risk individuals because of risk of abutment failure. [1] Atrophied and erythematous mucosa and or resected jaw bones inhibits the placement of removable prosthesis. Thus the overall morbidity due to cancer therapy is added with failure to replace and restore satisfactory mastication leads to decreased quality of life.

The implantation of tooth / biomaterials has emerged as a promising field in restorative dentistry. This article focuses on the efficiency of dental implants in irradiated bones.


 > History Top


An endosteal implant (implants embedded into bone) is an alloplastic material surgically inserted into a residual bony ridge primarily as a prosthodontic foundation [2] and is the most preferred implant compared to its counterparts like transosteal and periosteal implants.

The history of root form endosteal implants dates back thousands of years. The Chinese carved and implanted bamboo sticks in jaw bones 4000 years ago. Egyptians used precious metals 2000 years ago and Maggiolo used gold in 1809. The Mayan civilization has been shown to have used the earliest known examples of endosseous implants, dating back to over 1,350 years. [3]

In 1952, the Swedish orthopedic surgeon, Brånemark, while studying bone healing and regeneration, on animal and human subjects confirmed a unique property of titanium. Brånemark termed it as 'osseointegration". [4] Dr. Linkow known as the father of modern implant dentistry placed 19000 dental implants from 1952 to 2002. [3]


 > Healing Around Dental Implant Top


An adequate osseointegration is dependent on implant acceptance by living tissues as well as functional bone formation in the so-called bone-dental implant interface. The healing of this interface depends on biological and systemic patient-related issues, [5],[6],[7] implant design, [8],[9] load distribution between bone and implant [9],[10] and the surgical procedure. [11],[12]

The healing of the injured tissues after the insertion of a dental implant begins with the formation of a fibrin clot that detains the blood flow and gives initial support to the osteoprogenitor cells. The adequate formation of this clot determines the direct and stable connection between bone and implant, i.e. osseointegration. [13]

With the osseointegration ends a series of biological processes of tissue repair started with the injury caused during the surgical procedure of implant placement.

Bio physical and biochemical analyses of long-term experimental and clinical observation indicate that there is an active interchange between the implanted titanium fixture and soft and hard tissues, which eventually results in improved anchorage. [12]


 > Altered Bone Physiology in Irradiated Patients Top


The reaction of bone after irradiation is either circulatory or metabolic. [14] Initially, the circulatory hyperemic effect dominates; later, the metabolic changes become more significant. The metabolism increases in spite of decreased blood flow, secondary to vascular damage, due to the reactive cell surface in remodeling. This concept is supported by an early enzymatic increase after irradiation. [15] Thus an interaction of cellular, vascular, and metabolic alterations occurs in the different components of bone and in the adjacent tissues.

The intensity of the reactions is highly variable and may be partly dose related, although it is also influenced by many other parameters related to radiation delivery. This often is a reversible process which has the potential to turn into severe and irreversible alterations such as bone necrosis.

All of the components of the irradiated bone have different degrees of sensitivity to radiation. Mineral bone is not considered to be radiosensitive. Non-mineralized elements such as the cartilage plate in growing bones, marrow cells, and osteogenic cells, are radiosensitive. [16] The initial changes in bone result from depletion of the osteocyte population. Osteoblasts tend to be more radiosensitive than osteoclasts, so that after a course of radiotherapy there may be a disproportionally larger lytic activity. With excessive depletion of the osteocyte population regions of the bone become devitalized and degenerative changes begin to develop. These changes are potentiated because the same doses of radiation will injure the small blood vessels of the bone as well as the oral mucosa. [17] Radiation results in a decrease in qualitative osteoblast activity with reduced alkaline phosphatase activity. [18] The periosteum is also affected by this loss of cellularity, vascularity, and osteoid formation. [19]

Tolerance is greater for fractionated dose irradiation, than for single exposures to the same levels. [16]

Jacobson et al, [20] in a study on rabbits quantifies the bone regenerative capacity directly after administration of 15 Gy 60 Co irradiation. It was found that bone regeneration was depressed by 70.9% within a four-week period after irradiation. At a follow-up of one year, the average depression of bone-forming capacity was only 28.9%. This means a recovery by a factor of almost 2.5 in 12 months. Hence he advocates reconstruction and insertion of dental implants will be more successful with longer time span between irradiation and surgery.

Irradiation leads to the formation of hypoxic-hypocellular and hypovascular tissue, and then to the breakdown of tissue driven by persistent hypoxia which can cause a chronic nonhealing wound. [21] This damage can cause cell death. Functional loss of salivary gland tissues if in the radiated volume along with the presence of carious teeth or any oral or systemic bacterial infection enormously increases the risk of mandibular osteoradionecrosis (ORN). [21]


 > Animal Studies Top


Laboratory [22] and clinical [23],[24],[25] studies of titanium implants in irradiated bone have been conducted in rabbits. The bone formation on hydroxyapatite (HA) implant surface has been observed to occur earlier than on titanium impants. [26] HA is also a more biocompatible material than titanium. [27]

This finding is also supported by the histologic and histomorphometric analysis of bone remodeling in rabbits. More trabecular bone was present around the HA implant in controls than in the irradiated groups. If more trabecular bone is present around the implant, more force can be absorbed by the cancellous bone area. Therefore, HA implants in irradiated bone should be placed so that bearing by the cortical bone area is increased, for example, bicortically. [28] However according to Schon et al, [29] in the rabbit, osseointegration of an HA implant was found to be less efficient than that of a titanium implant.

The histologic effects of postimplantation irradiation on hydroxyapatite (HA)-bone contact have been investigated in several experimental studies. Schon et al[29] evaluated the tissue reaction around HA implants placed in the mandible of the rabbit five days before irradiation with a single 15-Gy 60 Co dose. In their study, two of the eight HA implants failed to contact the bone directly. Weinlander et al, [30] concluded that post implantation radiation had a deleterious effect on implant-bone contact. In his study, radiotherapy consisted of a dose equivalent to 5,000 cGy delivered in four fractions over a two-week period, and was started three weeks postimplantation. Khateery et al, [31] investigated the influence of radiotherapy (2,250 cGy in three doses over five days) on subperiosteal HA coated implants in rabbits. In contrast to the findings of Schön et al, [29] and Weinlander et al, [30] they observed that the amount of bone formation around the implant was significantly greater in the irradiated sites.

To clear these differences Kudo et al, [32] histologically and histomorphometrically studied the effect of radiation in rabbits irradiated at three different time points after placement of implants. He concluded that therapeutic irradiation shortly after implantation inhibits direct contact between the HA implant and the surrounding bone. Regardless of the interval between implantation and irradiation, postimplantation irradiation inevitably delays bone remodeling.

According to Asikainen et al, [33] bone remodeling can occur only when irradiation is fractioned, because this leads to higher tissue tolerance .

The therapeutic timing and length of delay between irradiation and implantation appear decisive to ensure the correct osteogenic reaction and thus osseointegration. This delay adapted from the present animal model corresponds to a six-month period after radiotherapy. [34] A similar observation was found in the histological analysis of the mandibular bone of dogs 24 weeks after implantation. There was a higher level of remodeling in the irradiated animals than in the non-irradiated ones. [35]

Shirota et al[36] in their study on rats observed that aging is an important factor in prognosis of the HA implant in irradiated bone.

A tumoricidal dose of 4,500 rads in ten fractions delivered to the mandibles of rhesus monkeys produced clinically observable changes similar to those seen in human patients (namely mucositis. inability to eat, xerostomia). Microscopically, changes included loss of osteocytes from bone lacunae in Haversian bone but not in cancellous bone, changes in the cellularity and vascularity of the periosteum, fibrosis with loss of principal fiber arrangements and decrease of vessels in interstitial spaces. Marrow showed fibrosis with obliterative endarteritis, loss of hematopoiesis and proliferation of new bone. Narrowing or obliteration of blood vessels and plugging of some canals with osteoid were changes observed in the Haversian canals. [37]


 > Human Studies Top


Placement of implants pre or post radiotherapy:

The results of Schepers et al's [38] study show that implants, primarily inserted during ablative surgery and exposed to a range of radiation doses, have an equal chance of becoming functional when compared to implants that received no radiation. The success rate of osseointegration was 97% in the postoperative irradiated group and 100% in the non-irradiated group. Rehabilitation can start early and problems related to postoperative radiotherapy may be prevented. A large part of the integration will occur in the period between surgery and radiotherapy, i.e. within four to six weeks. [39] In a healthy mandible, the whole integration process will take close to three months. Primary implant placement may have the following advantages over secondary implant placement. (a) Implant-surgery in a, due to radiotherapy, compromised area is avoided thus reducing the risk of late complications, i.e. osteoradionecrosis, (b) early rehabilitation of speech and swallowing, and (c) another surgical intervention and need for adjunctive HBO therapy can be avoided.

Schoen [40] too recommends insertion of implants immediately following the ablative procedure during the same surgical session when postoperative radiotherapy is indicated. A major disadvantage of immediate implant insertion concerns the risk of improper implant positioning. This impairs the prosthodontic treatment and can sometimes even not be used in the prosthodontic rehabilitation of a patient. [41] Other disadvantages include the risk of interference with or delay of the oncological therapy including radiation therapy, and the development of post-treatment complications caused by implantation being performed during ablative surgery. [41] These disadvantages are assessed to be of minor importance because of the very low incidence and morbidity, especially when compared to the high risk of harmful tissue reactions in the case of implantation after radiotherapy. [42] A two-stage technique is advocated to minimize the risk of early post-ablative complications as the implants are covered by mucosa during radiation therapy. Finally, by using multiple radiation fields, backscatter doses can be minimized and are of negligible clinical relevance. [43]

It is shown that implants placed after finishing postoperative radiotherapy, osseointegrate well depending on the total dose of radiotherapy. [44],[45],[46],[47],[48],[49],[50],[51] Up to 35% of the implants secondarily placed in irradiated mandibular bone are reported to be lost because of problems in osseointegration. [52]

Nelson [53] used different implant systems with different surface topographies (acid-etching and airborne-particle abrasion) and found these to have an equivalent osseointegration potential.

Werkmeister et al, [51] advocate the abandonment of non vascularized bone graft whenever implant placement is planned in irradiated areas.

Eckert et al, [54] studied the success of endosseous implants in irradiated tissue bed. The results demonstrate a higher implant survival rate in the mandible as compared to maxillae.

In a pilot study on quality of life assessment in implant retained prosthetically reconstructed maxillae and mandibles, Dholam et al, [55] attributed radiation of the tissues as the primary cause of failures in implants at stage I and II of implant surgery. They also found peri-implantitis and proliferative growth around implants in skin grafted mucosa.

Radiation dose

Colella et al, [56] in a review on implants in radiated bones found that no failures were observed in association with an radiation dose lower than 45 Gy. All implant failures observed occurred within 36 months after radiation, and most occurred between one and twelve months after placement.

Location and site of Implants in jaws

Roumanas et al, [57] demonstrated by location an implant success rate of 80% in the anterior maxilla and 66% in the posterior maxilla in radiated patient.

Nishimura [47] observed that in clinical practice, most patients irradiated for head and neck tumors do not receive radiation to the symphyseal region. Therefore implants can be placed in this region with a high degree of predictability when it is out of the field of irradiation. The risks of osteoradionecrosis (ORN) should be considered when this region is in the treatment field. In the maxilla, the risk of bone necrosis is probably negligible due to its diffuse blood supply and larger treatment volume when irradiated. The implants placed into the irradiated anterior mandible have demonstrated an acceptable implant success rate of 94% to 100% with a minimal risk of osteoradionecrosis. The efficacy of implants in the posterior mandible has not been examined. Implant success rates ranged from 69% to 95% in the irradiated maxilla for intraoral applications.

Timing of implant placement

Jacobson et al, [58] recommended that dental implantation should be done at least after one year of completion of radiation. Taylor et al, [59] and Franzen et al, [60] believe that implant placement should be delayed at least two years after completion of irradiation therapy. The results of animal experiments in Gothenburg [58] suggest that some revascularization of irradiated bone will occur longitudinally and that a delay of two or more years is beneficial. The additional time after tumor therapy also reduces the risk of tumor recurrence. Wagner et al, [61] feel that the time interval between irradiation and dental implantation should be 15 months and the time interval between implantation and reconstruction four months.

Timing of abutment placement and loading the implants

Taylor et al, [59] assume that bone healing and osseointegration occur at a slower rate than in normal tissue. For this reason abutment connection should be delayed for six months. Loading of the soft tissues in the area of the surgical site should be avoided completely during the healing phase.

Branemark et al, [4] advocated an unloaded healing time of three to six months. This is in contrast to the implant loading protocols, progressive loading [62] and immediate loading. [63] A healing period without loading is currently still considered as a prerequisite for implant integration. This leads to extended treatment periods often with delayed functional improvement for the patient. [64],[65],[66],[67],[68] Early loading has been found to induce micromotions at the bone-implant interface that may lead to a fibrous encapsulation instead of direct bone apposition. [66],[67]

Type of prosthesis

Cuesta-Gil [69] advocate placement of a single type of prosthesis-in most cases implant-retained overdentures. These prostheses facilitate occlusal fitting, require fewer implants, facilitate gingival hygiene, distribute the occlusal forces (thereby avoiding stress on the implants), and are less expensive. Fixed prostheses are less indicated in such patients because the treatment involved is more complex and costly and requires a larger number of implants (with perfect placement). Moreover, occlusal fitting is more difficult, hygiene, and the follow-up is poorer of implants and there is the possibility of oncologic disease relapse. Meijer et al, [70] recommended fixed dentures on only two implants in irradiated edentulous patients. Their philosophy is that, it minimizes the trauma of placing four implants in radiated patients and reduces the chewing force. Trismus and mucosal conditions make it difficult to achieve sufficient vertical dimension for four implant supported over denture.

Fixed partial dentures in the mandible appear to be a feasible alternative in fully edentulous head and neck cancer patients after ablative cancer surgery and irradiation therapy. With respect to implant survival, there is ample support for the hypothesis that fixed prostheses lead to higher success rates than removable ones. [71]

Success and failure of implants

Success and failure rate of implants in irradiated bone by various authors is mentioned in [Table 1].
Table 1: Implant failure rate by various authors

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 > Use of Hyperbaric Oxygen Top


Hyperbaric oxygen (HBO) is defined as the breathing of oxygen under increased pressure in a pressure chamber (two to three atmospheres absolute). HBO inhibits leukocyte adhesion to endothelium, diminishing tissue damage, and enhances leukocyte motility, resulting in improved microcirculation. [72] In the short term, this causes an increase in the tissue's internal oxygen pressure, leading to vasoconstriction, enhanced oxygen delivery, edema reduction, phagocytose activation, and an anti-inflammatory effect. [73]

The long-term effects are neovascularization, osteogenesis, and a stimulation of collagen production by fibroblasts, which promote wound healing.

The European Committee for Hyperbaric Medicine categorized the use of HBO in ORN of mandible as "strongly recommended" and surgery and implant in irradiated tissue as "recommended". [72]

Marx, [21] the founder of the so-called 3H model (hypoxia, hypocellularity, hypovascularity) of the pathogenesis of ORN, has introduced 'Marx protocol' for HBO and implants. He suggests 20 "dives" before treatment and 10 "dives" after treatment of osseointegrated implants. Larsen [74] too supports this regimen.

Arcuri [75] states that the success of osseointegration with HBO was 94% in his study.

In contrast, Keller [76] does not advocate the use of adjuvant HBO therapy in view of economic factors, potential complications of HBO therapy, and the low incidence of complications without its use.

Granstrom et al, [77] recommends adjuvant HBO for reducing the failure rate of implants in irradiated bone.

Barber et al, [78] concluded that factors such as the graft having its own blood supply and the use of HBO contributed to the successful osseointegration of these implants.

There is only one randomized controlled trial conducted by Schoen et al, [79] reported in the Cochrane review. [80] The outcome of this trial showed that there was no clinical significant difference between HBO treated and non-HBO treated patients with regard to implant success. The better performance was shown by patients not treated with HBO on almost every aspect of this controlled trial. A possible explanation was the extra treatment burden encompassing thirty sessions of HBO, affecting quality of life. The study population of this trial was small, and a very large population is needed to detect the usefulness of HBO therapy. It is doubtful, however, whether such a large randomized controlled trial will actually prove effective, and the clinical use of HBO is remarkable considering the existing opposing views on its efficacy and value.

Experimental research in the last two decade regarding the effect of HBO therapy on previously irradiated head and neck tissue is scarce. It is therefore concluded that more research, both clinical and experimental, is necessary before conclusions can be drawn.


 > Discussion Top


Implant material : Most of the studies are on titanium implants. [38],[40],[42],[43],[44],[45],[46],[47],[48],[49],[50],[51] The hydroxyapatite coated implants are also found to be successful mainly because of its rough surface and the osseoconductive properties of hydroxyapatite. [29] Advanced dental implant surfaces like TPS [titanium plasma spreaded], SLA [sandblasted and acid etched], Ti-Unite and different implant materials like zirconia [zirconium oxide] have showed comparable results in non irradiated bones but long-term evaluation and studies are required to judge their survival rate in irradiated bones.

Implant position : With regard to the anatomical position, implants can be best placed in the mandibular anterior / symphyseal region [success rate of 94% to 100%] as it is the area which receives the least amount of radiation. [47] The ability of the anterior mandible to maintain viable bone, even when the posterior regions are highly radiated was demonstrated by Gowgiel. [81] It is also found to be the safest area of the mandible as far as osseointegration is concerned followed by the mandibular premolar region and the maxillary jaw. The maximum implant failures are reported in the maxillary jaw [69% to 95%] [47] which is least prone to ORN because of its diffuse blood supply and cancellous bone.

Werkmeister et al, [51] advocate the abandonment of non vascularized bone graft whenever implant placement is planned in irradiated areas. Hence insertion of implants in vascularized bone grafts is advocated.

Type of prosthesis : Fixed implant supported prosthesis is advocated in irradiated mandibles. The implant supported over dentures is better in vascularized or non-vascularized grafted patients. Fixed over denture type of prosthesis is advised by Meijer et al, [70] supported by two implants.

Effect of radiation dose : The radiation dose has an effect on osseointegration. Favorable osseointegration is found in radiation doses lesser than 45-50 Gy. [56]

Type of irradiation source : Most studies published on osseointegration in irradiated tissues have used 60 Co as the source for radiotherapy. With the development of higher energy radiotherapy protocols and superfractionation, it is likely that in time other effects on osseointegration will be identified. Brachytherapy is also a part of oncologic treatment, and its effect on bone tissues is different from external beam radiotherapy. Again, too little is known about its effect on osseointegration today.

Effect of smoking : Smoking has negative effects on osseointegrtaion. [82] The vasoconstriction and vascular damage which causes decreased vascular supply lead to implant failure. A smoking cessation protocol [82] before implant placement is accepted globally. Hence radiated patients who continued to smoke must be considered as an absolute contraindication to treatment.

Soft tissue complications : Soft tissues around implants behave differently in radiated bones than in non radiated bones. Eckert et al, [54] noted that significant problems in patients with irradiated implants were related to the soft tissues. Gingivitis was more common in these patients than normally observed. Cover-screw mucosal perforations were observed over the areas of 17% of implants during the healing period between stage one and stage two surgery.

August et al, [44] reported increased problems with the soft tissues. Early soft tissue complications included soft tissue overgrowth, tongue ulceration, and intraoral wound dehiscence. Late complications included fistula formation.

Dholam [55] also found soft tissue complications especially irradiated osteomyocutaneous grafted patients.

Primary vs secondary implant placement

More predictable osseointegration has been reported with primary placement of implants before radiotherapy. [38],[39] The cost factor, improper positioning of implants, and the late effects of treatment (surgery, radiation) like fibrosis inducing trismus, favor secondary placement. The patient too, by this time, is aware of the altered physical and physiological state and accepts the shortcomings and is psychologically prepared to extend the treatment and get rehabilitated.

Hyperbaric oxygen

The use of HBO is still controversial. Some studies found it useful [74],[75],[77] while others considered it as an additional burden of treatment. [76],[79] The studies failed to prove cost effectiveness of HBO as a supportive care in implant osseointegration.

Timing of implant placement

One year time interval between tumor therapy and the time of dental implantation as recommended by Jacobson [58] seems logical. This period facilitates the tissues to recover from the immediate side effects of radiation and the bone remodeling and vascularization to set in. The patient is rehabilitated in a reasonable time period too.

Timing of abutment placement and loading the implants

Abutment connection, fabrication and loading of the prosthesis should be delayed for six months instead of the traditional three to four months to permit osseointegration. [64],[65],[66],[67],[68] This extra time period assists in achieving uninterrupted and unloaded osseointegration.


 > Conclusions Top


Factors which contribute to the success of implant retained oral rehabilitation in radiated patient are careful selection of patients after evaluating the clinical conditions and results following surgery, reconstruction, radiation, prognosis and the cost factor. Insertion of implant should be undertaken after one year of radiation and attachment of abutment and prosthesis fabrication after six months of insertion of implant. This period is necessary to achieve osseointegration after receiving radiation. Placement of a minimum number of implants is advocated. Prosthesis can be fabricated on two implants. Fabrication of over denture in radiated jaw and fixed denture in microvascular grafted jaw is advocated. Insertion of implants should be preferably done in microvascular grafted jaws.

Hydroxyapatite-coated titanium implants is the material of choice today. Increased failure rates are observed when the radiation dose exceeds 45Gy. The implant success rate is higher in the mandibular symphyseal region followed by the mandibular posterior region and least maxilla. To assess the effects of HBO treatment on acceleration of osseointegration, more randomized trials are required. [83]

 
 > References Top

1.Rosenstieal SF, Land MF, Fujimoto J. History taking and clinical examination. In: Rosenstieal SF, Land MF, Fujimoto J, editors. Contemporary fixed prosthodontics. 4 th ed. St. Louis, Missouri: Mosby; 2007. p. 3-42.  Back to cited text no. 1
    
2.AAID Nomenclature Committee. Glossary of implant terms. J Oral Implantol 1990; 16:57-63.  Back to cited text no. 2
    
3.Wikipedia.org [internet]. Wikipedia foundation,inc.; [updated 2011 April 14]. Available from: http://www.en.wikipedia.org/wiki/Dental_implant/. [Last cited on 2011 Apr 18].  Back to cited text no. 3
    
4.Brånemark PI, Hansson BO, Adell R, Breine U, Lindström J, Hallén O, et al. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period. Scand J Plast Reconstr Surg Suppl. 1977;16:1-132.  Back to cited text no. 4
    
5.Schenk RK, Burser D. Osseointegration: A reality. Periodontol 2000. 1998;17:22-35.   Back to cited text no. 5
    
6.Albrektsson T, Johansson C. Osteoinduction, osteoconduction and osseointegration. Eur Spine J 2001;10 (Suppl 2):S96-101.  Back to cited text no. 6
    
7.Cooper LF. Biologic determinants of bone formation for osseointegration: Clues for future clinical improvements. J Prosthet Dent. 1998;80:439-49.  Back to cited text no. 7
    
8.Matsuno H, Yokoyama A, Watari F, Uo M, Kawasaki T. Biocompatibility and osteogenesis of refractory metal implants, titanium, hafnium, niobium, tantalum and rhenium. Biomaterials 2001;22:1253-62.  Back to cited text no. 8
    
9.Gapski R, Wang HL, Mascarenhas P, Lang NP. Critical review of immediate implant loading. Clin Oral Implants Res 2003;14:515-27.   Back to cited text no. 9
    
10.Sikavitsas VI, Temenoff JS, Mikos AG. Biomaterials and bone mechanotransduction. Biomaterials 2001;22:2581-93.  Back to cited text no. 10
    
11.Fragiskos FD, Alexandridis C. Osseointegrated implants. In: Fragiskos FD, editor. Oral Surgery. Berlin, Heidelberg: Springer; 2007. p. 337-48.  Back to cited text no. 11
    
12.Brånemark PI. Osseointegration and its experimental background. J Prosthet Dent 1983;50:399-410.  Back to cited text no. 12
    
13.Vanegas-Acosta JC, Landinez P NS, Garzón-Alvarado DA. Mathematical model of the coagulation in the bone-dental implant interface. Comput Biol Med 2010;40:791-801.  Back to cited text no. 13
    
14.King MA, Casarett GW, Weber DA. A study of irradiated bone: I. histopathologic and physiologic changes. J Nucl Med 1979;20:1142-9.  Back to cited text no. 14
    
15.Aitasalo K. Effect of irradiation on early enzymatic changes in healing mandibular periosteum and bone. A histochemical study on rats. Acta Radiol Oncol 1986;25:207-12.  Back to cited text no. 15
    
16.Rubin P. Regeneration of bone marrow in rabbits following local, fractionated irradiation. Cancer 1973;32:847-52.  Back to cited text no. 16
    
17.Keys HM, McCasland JP. Techniques and results of a comprehensive dental care program in head and neck cancer patients. Int J Radial Oncol Biol Phys 1976;1:859-65.   Back to cited text no. 17
    
18.Dudziak ME, Saadeh PB, Mehrara BJ, Steinbrech DS, Greenwald JA, Gittes GK, et al. The effects of ionizing radiation on osteoblast-like cells in vitro. Plast Reconstr Surg 2000;106:1049-61.  Back to cited text no. 18
    
19.Güngör T, Hedlund T, Hulth A, Johnell O. The effect of irradiation on osteoclasts with or without transplantation of hematopoietic cells. Acta Orthop Scand 1982;53:333-7.  Back to cited text no. 19
    
20.Jacobsson MG, Jönsson AK, Albrektsson TO, Turesson IE. Short- and long-term effects of irradiation on bone regeneration. Plast Reconstr Surg 1985;76:841-50.  Back to cited text no. 20
    
21.Marx RE. Osteoradionecrosis: A new concept of its pathophysiology. J Oral Maxillofac Surg 1983;41:283-8.  Back to cited text no. 21
    
22.Schweiger JW. Titanium implants in irradiated dog mandibles. J Prosthet Dent 1989;62:201-5.  Back to cited text no. 22
    
23.Tjellström A, Rosenhall U, Lindström J, Hallén O, Albrektsson T, Brånemark PI. Five-year experience with skin-penetrating bone-anchored implants in the temporal bone. Acta Otolaryngol 1983;95:568-75.  Back to cited text no. 23
    
24.Jacobsson M, Tjellström A, Thomsen P, Albrektsson T, Turesson I. Integration of titanium implants in irradiated bone. Histologic and clinical study. Ann Otol Rhinol Laryngol 1988;97:337-40.  Back to cited text no. 24
    
25.Parel SM, Tjellström A. The United States and Swedish experience with osseointegration and facial prostheses. Int J Oral Maxillofac Implants 1991;6:75-9.  Back to cited text no. 25
    
26.Block MS, Kent JN, Kay JF. Evaluation of hydroxylapatite-coated titanium dental implants in dogs. J Oral Maxillofac Surg 1987;45:601-7.  Back to cited text no. 26
    
27.Osborn JF, Newesely H. Dynamic aspect of the Implant -bone interface. In: Osborn, editors. Dental implants. Munchen: Carl Hanser Verlag; 1980. p. 111-23.  Back to cited text no. 27
    
28.Matsui Y, Ohno K, Michi K, Tachikawa T. Histomorphometric examination of healing around hydroxylapatite implants in 60Co-irradiated bone. J Oral Maxillofac Surg 1994;52:167-72.  Back to cited text no. 28
    
29.Schön R, Ohno K, Kudo M, Michi K. Peri-implant tissue reaction in bone irradiated the fifth day after implantation in rabbits: Histologic and histomorphometric measurements. Int J Oral Maxillofac Implants 1996;11:228-38.  Back to cited text no. 29
    
30.Weinlander M, Beumer J, Nishimura R. Histological and histomorphometrical evaluation of implant-bone interface after radiation therapy. Presented at the Fifth International Congress on Pre-Prosthetic Surgery; 1993 April 15-18; Vienna, Austria. 1993 (abstr).  Back to cited text no. 30
    
31.Khateery S, Waite PD, Lemons JE. The influence of radiation therapy on subperiosteal hydroxyapatite implants in rabbits. J Oral Maxillofac Surg 1991;49:730-4.  Back to cited text no. 31
    
32.Kudo M, Matsui Y, Ohno K, Michi K. A histomorphometric study of the tissue reaction around hydroxyapatite implants irradiated after placement. J Oral Maxillofac Surg 2001;59:293-300; discussion 301.  Back to cited text no. 32
    
33.Asikainen P, Klemetti E, Kotilainen R, Vuillemin T, Sutter F, Voipio HM, et al. Osseointegration of dental implants in bone irradiated with 40, 50 or 60 gy doses. An experimental study with beagle dogs. Clin Oral Implants Res 1998;9:20-5.  Back to cited text no. 33
    
34.Brogniez V, Lejuste P, Pecheur A, Reychler H. Dental prosthetic reconstruction of osseointegrated implants placed in irradiated bone. Int J Oral Maxillofac Implants 1998;13:506-12.  Back to cited text no. 34
    
35.Brasseur M, Brogniez V, Grégoire V, Reychler H, Lengelé B, D'Hoore W, Nyssen-Behets C. Effects of irradiation on bone remodelling around mandibular implants: An experimental study in dogs. Int J Oral Maxillofac Surg 2006;35:850-5.  Back to cited text no. 35
    
36.Shirota T, Donath K, Ohno K, Matsui Y, Michi K. Effect of age and radiation on bone healing adjacent to hydroxyapatite placed in the tibia of rats. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995;79:285-94.  Back to cited text no. 36
    
37.Rohrer MD, Kim Y, Fayos JV. The effect of cobalt-60 irradiation on monkey mandibles. Oral Surg Oral Med Oral Pathol 1979;48:424-40.  Back to cited text no. 37
    
38.Schepers RH, Slagter AP, Kaanders JH, van den Hoogen FJ, Merkx MA. Effect of postoperative radiotherapy on the functional result of implants placed during ablative surgery for oral cancer. Int J Oral Maxillofac Surg 2006;35:803-8.   Back to cited text no. 38
    
39.Schoen PJ, Reintsema H, Raghoebar GM, Vissink A, Roodenburg JLN. The use of implant retained mandibular prostheses in the oral rehabilitation of head and neck cancer patients. A review and rationale for treatment planning. Oral Oncol 2004;40:862-71.  Back to cited text no. 39
    
40.Schoen PJ, Raghoebar GM, Bouma J, Reintsema H, Burlage FR, Roodenburg JL, et al. Prosthodontic rehabilitation of oral function in head-neck cancer patients with dental implants placed simultaneously during ablative tumour surgery: An assessment of treatment outcomes and quality of life. Int J Oral Maxillofac Surg 2008;37:8-16.   Back to cited text no. 40
    
41.Sclaroff A, Haughey B, Gay WD, Paniello R. Immediate mandibular reconstruction and placement of dental implants. At the time of ablative surgery. Oral Surg Oral Med Oral Pathol 1994;78:711-7.  Back to cited text no. 41
    
42.Granström G, Bergström K, Tjellström A, Brånemark PI. A detailed study of titanium implants lost in irradiated tissues. Int J Oral Maxillofac Implants 1994;9:653-62.  Back to cited text no. 42
    
43.Wang R, Pillai K, Jones PK. Dosimetric measurement of scattered radiation from dental implants in simulated head and neck radiotherapy. Int J Oral Maxillofac Implants 1998;13:197-203.  Back to cited text no. 43
    
44.August M, Bast B, Jackson M, Perrott D. Use of fixed mandibular implant in oral cancer patients. J Oral Maxillofac Surg 1998;56:297-301.  Back to cited text no. 44
    
45.Harrison JS, Stratemann S, Redding SW. Dental implants for patients who have had radiation treatment for head and neck cancer. Spec Care Dentist 2003;23:223-9.  Back to cited text no. 45
    
46.Mericske-Stern R, Perren R, Raveh J. Life table analysis and clinical evaluation of oral implants supporting prostheses after resection of malignant tumours. Int J Oral Maxillofac Implants 1999;14:673-80.  Back to cited text no. 46
    
47.Nishimura RD, Roumanas E, Beumer J, Moy PK, Schimizu KT. Restoration of irradiated patients using osseointegrated implants: Current perspectives. J Prosthet Dent 1998;79:641-7.  Back to cited text no. 47
    
48.Gbara A, Darwich K, Li L, Schmelzle R, Blake F. Long-term results of jaw reconstruction with microsurgical fibula grafts and dental implants. J Oral Maxillofac Surg 2007;65:1005-9.  Back to cited text no. 48
    
49.Visch LL, van Waas MA, Schmitz PI, Levendag PC. A clinical evaluation of implants in irradiated oral cancer patients. J Dent Res 2002;81:856-9.  Back to cited text no. 49
    
50.Weischer T, Mohr C. Ten year experience in oral implant rehabilitation of cancer patients: Treatment concept and proposed criteria for success. Int J Oral Maxillofac Implants 1999;14:521-35.  Back to cited text no. 50
    
51.Werkmeister R, Szulczewski D, Walteros-Benz P, Joos U. Rehabilitation with dental implants of oral cancer patients. J Craniomaxillofac Surg 1999;27:38-41.  Back to cited text no. 51
    
52.Kwakman JM, Freihofer HP, van Waas MA. Osseointegrated oral implants in head and neck cancer patients. Laryngoscope 1997;107:519-22.  Back to cited text no. 52
    
53.Nelson K, Heberer S, Glatzer C. Survival analysis and clinical evaluation of implant-retained prostheses in oral cancer resection patients over a mean follow-up period of 10 years. J Prosthet Dent 2007;98:405-10.  Back to cited text no. 53
    
54.Eckert SE, Desjardins RP, Keller EE, Tolman DE. Endosseous implants in an irradiated tissue bed. J Prosthet Dent 1996;76:45-9.  Back to cited text no. 54
    
55.Dholam KP, Bachher GK, Yadav PS, Quazi GA, Pusalkar HA. Assessment of quality of life after implant-retained prosthetically reconstructed maxillae and mandibles postcancer treatments. Implant Dent 2011;20:85-94.  Back to cited text no. 55
    
56.Colella G, Cannavale R, Pentenero M, Gandolfo S. Oral implants in radiated patients: A systematic review. Int J Oral Maxillofac Implants 2007;22:616-22.  Back to cited text no. 56
    
57.Roumana ED, Nishimura RD, Davis BK, Beumer J 3 rd . Clinical Evaluation of implant retaining edentulous maxillary obturator prostheses. J Prosthet Dent 1997;77:184-90.  Back to cited text no. 57
    
58.Jacobsson M. On bone behavior after irradiation [Thesis]. Swaden: University of Gothenburg; 1985.  Back to cited text no. 58
    
59.Taylor TD, Worthington P. Osseointegrated implant rehabilitation of the previously irradiated mandible: Results of a limited trial at 3 to 7 years. J Prosthet Dent 1993;69:60-9.  Back to cited text no. 59
    
60.Franzèn L, Rosenquist JB, Rosenquist KI, Gustafsson I. Oral implant rehabilitation of patients with oral malignancies treated with radiotherapy and surgery without adjunctive hyperbaric oxygen. Int J Oral Maxillofac Implants 1995;10:183-7.   Back to cited text no. 60
    
61.Wagner W, Esser E, Ostkamp K. Osseointegration of dental implants in patients with and without radiotherapy. Acta Oncol 1998;37:693-6.  Back to cited text no. 61
    
62.Misch CE. Progressive bone loading. In: Misch CE, editor. Dental Implant Prosthetics. St Louis, MO: Elsevier Mosby; 2005; 26:511-530.  Back to cited text no. 62
    
63.Misch CE, Scortecci GM. Immediate load application in implant dentistry. In: Misch CE, editor. Dental Implant Prosthetics. St. Louis, Missouri: Elsevier Mosby; 2005. p. 531-67.  Back to cited text no. 63
    
64.Jacobson M, Tjellstrom A, Fine L, Anderson H. A retrospective study of osseointegrated skin-penetrating titanium fixtures used for retaining facial prostheses. Int J Oral Maxillofac Implants 1994;9:653-62.  Back to cited text no. 64
    
65.Adell R, Lekholm U, Rockler B, Branemark PI. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981;10:387-416.  Back to cited text no. 65
    
66.Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long-term efficacy of currently used dental implants: A review and proposed criteria of success. Int J Oral Maxillofac Implants 1986;1:11-25.  Back to cited text no. 66
    
67.Albrektsson T, Sennerby L. State of the art in oral implants. J Clin Periodontol 199l;18:474-81.  Back to cited text no. 67
    
68.Salama H, Rose LF, Salama M, Betts NJ. Immediate loading of bilaterally splinted titanium root form implants in fixed prosthodontics-a technique re-examined: Two case reports. Int J Periodontics Restorative Dent 1995;15:345-61.  Back to cited text no. 68
    
69.Cuesta-Gil M, Ochandiano Caicoya S, Riba-García F, Duarte Ruiz B, Navarro Cuéllar C, Navarro Vila C. Oral rehabilitation with osseointegrated implants in oncologic patients. J Oral Maxillofac Surg 2009;67:2485-96.  Back to cited text no. 69
    
70.Meijer GJ, Mel P, Koole R, Cune MS. Fixed partial dentures on two implants: Raising comfort in irradiated edentulous patients. Int J Oral Maxillofac Surg 2007;36:646-8.  Back to cited text no. 70
    
71.Granstrom G. Osseointegration in irradiated cancer patients: An analysis with respect to implant failures. J Oral Maxillofac Surg 2005;63:579-85.  Back to cited text no. 71
    
72.Mortensen CR. Hyperbaric oxygen therapy. Curr Anaesth Crit Care 2008;19:333-7.  Back to cited text no. 72
    
73.Spiegelberg L, Djasim UM, van Neck HW, Wolvius EB, van der Wal KG. Hyperbaric oxygen therapy in the management of radiation-induced injury in the head and neck region: A review of the literature. J Oral Maxillofac Surg 2010;68:1732-9.  Back to cited text no. 73
    
74.Larsen PE. Placement of dental implants in the irradiated mandible: A protocol involving adjunctive hyperbaric oxygen. J Oral Maxillofac Surg 1997;55:967-71.  Back to cited text no. 74
    
75.Arcuri MR, Fridrich KL, Funk GF, Tabor MW, LaVelle WE. Titanium osseointegrated implants combined with hyperbaric oxygen therapy in previously irradiated mandibles. J Prosthet Dent. 1997;77:177-83.  Back to cited text no. 75
    
76.Keller EE. Placement of dental implants in the irradiated mandible: A protocol without adjunctive hyperbaric oxygen. J Oral Maxillofac Surg. 1997;55:972-80.  Back to cited text no. 76
    
77.Granström G, Tjellström A, Brånemark PI. Osseointegrated implants in irradiated bone: A case-controlled study using adjunctive hyperbaric oxygen therapy. J Oral Maxillofac Surg 1999;57:493-9.  Back to cited text no. 77
    
78.Barber HD, Seckinger RJ, Hayden RE, Weinstein GS. Evaluation of osseointegration of endosseous implants in radiated, vascularized fibula flaps to the mandible: A pilot study. J Oral Maxillofac Surg 1995;53:640-4.  Back to cited text no. 78
    
79.Schoen PJ, Raghoebar GM, Bouma J, Reintsema H, Vissink A, Sterk W, et al. Rehabilitation of oral function in head and neck cancer patients after radiotherapy with implant-retained dentures: Effects of hyperbaric oxygen therapy. Oral Oncol 2007;43:379-88.   Back to cited text no. 79
    
80.Coulthard P, Patel S, Grusovin GM, Worthington HV, Esposito M. Hyperbaric oxygen therapy for irradiated patients who require dental implants: A Cochrane review of randomised clinical trials. Eur J Oral Implantol 2008;1:105-10.  Back to cited text no. 80
    
81.Gowgiel JM. Experimental radio-osteonecrosis of the jaws. J Dent Res 1960;39:176-97.  Back to cited text no. 81
    
82.Bain CA. Smoking and implant failure--benefits of a smoking cessation protocol. Int J Oral Maxillofac Implants 1996;11:756-9.  Back to cited text no. 82
    
83.McGhee MA, Stern SJ, Callan D, Shewmake K, Smith T. Osseointegrated implants in the head and neck cancer patient. Head Neck 1997;19:659-65.  Back to cited text no. 83
    



 
 
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