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Keywords:

  • Dental implants;
  • oral cancer

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. References

Background:  Patients who undergo surgical management of oral cancer may greatly benefit from an implant-supported prosthesis. This study reports on the clinical experience of dental implant placement in patients following resection of oral cancer over a 15-year period. Controversies including the use of dental implants in irradiated tissues, and hyperbaric oxygen treatment will also be discussed.

Methods:  Thirty-one patients who had dental implants placed as part of their oral rehabilitation between 1992 and 2007 were investigated. Demographic data and factors including implant survival, type of prosthesis provided, radiotherapy and the hyperbaric oxygen therapy were analysed.

Results:  In this retrospective study, there was a retention rate of 110 implants from a total of 115 implants placed. A high rate of implant retention was found, with 5 implant failures from a total of 115 implants placed. The 5 failed implants occurred in free flap bone that had been irradiated.

Conclusions:  Dental implants provide an important role in the oral rehabilitation of oral cancer patients. There may be an increased risk of implant failure in free flap bone that has been irradiated.


Abbreviations and acronyms:
HBOT

hyperbaric oxygen treatment

ORN

osteoradionecrosis

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. References

The provision of dental implant based prosthodontic rehabilitation can significantly improve the quality of life for patients after oral cancer treatment.1 Such rehabilitation facilitates mastication, oral competence and facial support so that patients can speak, chew and appear in public with confidence.

Surgical management of oral cancer may lead to significant disability, including facial deformity, the loss of hard and soft tissue, impaired speech, swallowing, and mastication. Patients with extensive primary tumours often undergo chemotherapy and radiotherapy postoperatively,2 which may cause further morbidity that can adversely affect their quality of life.3

The head and neck is the seventh most common site of cancer in Victoria.4 Five-year survival rates are 59% for patients with oral cancer, and 69% of those treated for salivary gland cancer.4 Tumour stage at diagnosis and advanced age are factors that negatively influence prognosis.4 As a significant proportion of patients survive for five years after initial diagnosis, there is a need for adequate functional rehabilitation.

Rehabilitation with a removable prostheses can be difficult or impossible, due to distorted post-surgical anatomy (both static and functional), low salivary flow, and emotional resilience of the patient post-surgery. The expectations of the patient may not be realistic, and limited treatment goals such as aesthetic improvement may be all that are possible with a conventional removable prosthesis.

Some of the first applications of dental implants, described by Professor Brånemark in the 1970s, were used in reconstructing mandibular defects post-tumour resection.5,6 Implants provide stability, and support for a prosthesis, which limits pressure on soft tissues that may be compromised following surgery and radiotherapy.1 The stability and support afforded by dental implants reduces reliance on the patient’s oral coordination, which is particularly beneficial for patients who struggle to adapt to an oral prosthesis post cancer resection.1

Dental implant rehabilitation in oral cancer patients is challenging, requiring a multidisciplinary approach. A lack of residual bone following resection makes it difficult to place implants in an ideal position.1,7 Angled abutments and telescopic devices may be needed to enable attachment of the prosthesis (Fig 1).1,7 Transferred bone from distant sites such as the iliac crest or fibula may be required for implant placement in larger resections.7,8 This bone may be particulate, corticocancellous (Figs 2a and 2b), or free flap bone (Fig 3) harvested with its own blood supply.8 Soft tissue issues may also preclude the provision of implants, with bulky soft tissue flaps not allowing for maintenance of the peri-implant zone.

image

Figure 1.  This patient had maxillectomy 15 years earlier for adenoid cystic carcinoma. The image shows second stage surgery after placement of a telescopic custom abutment under a general anaesthetic. This custom abutment was used to enable attachment of a zygomatic implants supported maxillary obturator.

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image

Figure 2.  (a) This patient underwent bilateral maxillectomy and later had corticocancellous block bone grafts placed from the iliac crest. Corticocancellous bone graft form the iliac crest to allow later placement of dental implants into the grafted bone. (b) The same patient with implants placed into a corticocancellous bone graft. This patient subsequently had a functional removable prosthesis.

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image

Figure 3.  Implant-supported acrylic prosthesis placed into composite iliac crest free-flap bone. This composite free flap utilizes the iliac crest bone with muscle and skin based on the deep circumflex iliac artery and vein. This composite free flap has advantages in oral implants in providing ample width and depth of bone for osseointegrated implants.

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Patients who have had radiotherapy to the planned implant site are reported to have a reduced success rate.9,10 Previously, hyperbaric oxygen treatment (HBOT) has been recommended for these patients.11 However, the benefits are contentious.12

The purpose of this paper is to discuss the role and controversies of dental implants in the oral rehabilitation of head and neck cancer patients, and to audit our experience at the Royal Melbourne Hospital of implant placement in the jaws after oral cancer resection.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. References

Thirty-one patients who had oral implants placed between 1992 and 2007 as part of their oral rehabilitation post-cancer surgery were identified from a database and their records were reviewed. Only patients who underwent resection of malignant tumours and had dental implants placed were included in the study. Patients who underwent resection of benign but locally aggressive tumours were excluded. The 31 patients identified would constitute approximately 2% of all cancer patients seen during this period (from approximately 1500 patients). Information regarding the patient’s age, gender, cancer type, stage, and surgical management was noted. Other information, including smoking status, radiotherapy (type, dose and fractionation), and whether or not HBOT was used; implant type, site, and retention of the implant was recorded. The type and success of the final prosthesis, and long-term follow-up issues were also recorded.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. References

Clinical experience

From the 31 patients identified, a total of 115 Brånemark (Nobel Biocare) implants were placed. A two-staged implant placement protocol was used in all cases. The mean age at implant placement was 50.7 years with a range of 20–76 years (Table 1). The oral malignancies included 22 squamous cell carcinoma, 2 verrucous carcinoma, 4 osteosarcoma and 3 adenoid cystic carcinoma.

Table 1.   Clinical experience
Total patients 31
Mean age 50.7
Age range 20–76
Male 18
Female 13
Number of implants placed115
Retained110
Failed/removed implants  5
Implants not used  6

Of the 115 implants placed (in both irradiated and non-irradiated bone), 5 implants had to be removed within 2 years due to peri-implantitis, or non-integration. These 5 failed implants occurred in free flap bone in patients who received radiotherapy to the orofacial region after ablative cancer surgery. There were no failures in irradiated jaw bone, or irradiated block bone grafts.

Upper jaw implants

In the upper jaw, a total of 35 implants were placed. Twelve of these were placed into the remaining maxilla (post-cancer surgery). Eight zygomaticus implants were used in 3 patients where the maxilla had been resected. Six were placed into bone graft and 9 were placed into free flap bone (Table 2).

Table 2.   Upper jaw implants
Maxilla12
Free flap bone9
– iliac crest(4)
– fibula(5)
Bone graft6
Zygoma8
Total35

Lower jaw implants

In the lower jaw, a total of 80 implants were placed. Fifty-seven of these were placed into the remaining mandible, 23 in free flap bone, with 17 in iliac crest free flap bone and 6 into fibula free flap bone (Table 3).

Table 3.   Lower jaw implants
Mandible57
Free flap bone23
– iliac crest(17)
– fibula(6)
Total80

No implant failures occurred in jaw bone, in non-irradiated patients, or in irradiated bone grafts. There were also no implant failures in non-irradiated bone grafts. The 5 implant failures occurred in free flap bone that had been irradiated. Overall, the retention rate was 95.7%.

Implants in irradiated bone

In irradiated tissues, a total of 48 implants were placed. Eight implants were placed into the remaining maxilla, and 15 into free flap bone. Three were placed into zygoma and 22 into the remaining mandible. The 5 implant failures occurred in irradiated free flap bone giving a retention rate of 89.5% for irradiated bone and a 33.3% retention rate in irradiated free flap bone (Table 4). The mean time to implant removal was 8 months with a range of 4–18 months. All radiotherapy implant patients underwent hyperbaric oxygen treatment prior to implant placement, and the failed implants in these cases did not lead to osteoradionecrosis (ORN).

Table 4.   Implants in irradiated bone
Implant siteImplants placedFailed integration
Maxilla8
Free flap bone95
– DCIA(8)(3)
– fibula(7)(2)
Bone graft6
Zygoma3
Mandible22
Total48 retained5 removed

Prosthetic units

A total of 29 implant-supported prostheses were constructed. The main prostheses used were fixed prostheses utilizing a porcelain fused to metal framework (Fig 4) or fibre-reinforced acrylic framework. Implants were also used to support a dolder-bar or ball retained removable overdentures and obturators. These included 15 fixed bridge units, 10 over-dentures, 1 maxillary obturator and 3 partial dentures. Six implants were not utilized: 3 were left as sleepers, and the remaining 3 were not used because of an unfavourable position. Of note, 3 patients were unable to wear their prosthesis due to discomfort and an inability to tolerate the prosthesis, and 5 patients died before a prosthesis could be provided (Table 5).

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Figure 4.  Implant-supported porcelain fused to metal framework in a patient who had marginal mandibulectomy.

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Table 5.   Prosthetic units
Total units made29
– fixed bridge(15)
– overdenture(10)
– partial denture(3)
Patient unable to wear prosthesis3
Patient death before prosthesis fitted5

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. References

Patients with oral cancer require multidisciplinary management involving surgeons, radiation and medical oncologists, dental specialists and allied health specialists. Dental implants are an important component of multidisciplinary rehabilitation of oral cancer patients after surgical resection.

Of the three modalities of oral cancer treatment (surgery, radiotherapy and chemotherapy), surgery is most commonly used. The surgical defect can range from a small soft tissue deformity to a large defect where significant amounts of maxilla or mandible are lost. These larger defects require reconstruction with composite bone and soft tissue free flaps.8 In these larger resections, dental implants can provide a stable platform for an oral prosthesis. Whilst the aim of treatment is usually cure, palliative care is sometimes indicated for patients that have advanced disease or significant comorbidities.

The aim of post-cancer surgery is to restore form and function to the orofacial region. There are many factors to consider for the post-surgical patient. Oral-nasal competence is highly desirable for speech and swallowing. Soft tissues need to be adequately soft and pliable to allow natural movement if possible. The soft tissue overlying the bone where implants are to be placed must be thin and immobile over the bone to facilitate maintenance of the implants. The tongue space should not be encroached upon as this may impair speech and mastication. The oral aperture must be adequate to allow a normal range of mandibular motion and access for prosthesis fabrication and insertion, and for the insertion of food and eating implements. Limitation of mouth opening from scarring can make prosthetic rehabilitation challenging, if not impossible. An anatomical sulcus is helpful for mastication and management of food in the oral cavity and is important for the retention of a denture prosthesis (Fig 5). Implant-supported prostheses facilitate the support of soft tissue, and provide a stable platform for mastication and speech.1,7

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Figure 5.  Loss of anatomical sulcus creates a challenge in providing a removable oral prosthesis. Dental implants would provide anchorage for retention and stability of an oral prosthesis.

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If radiotherapy is used, multiple dental extractions are frequently carried out to lessen the need for later dental extractions, and thus reduce the incidence of ORN. The early complications of radiotherapy include mucositis, xerostomia and burns.1 Complications that can occur later include fibrosis, increased rates of infection, ORN, and implant failure.1 Patients who have already had extensive surgery (plus radiotherapy) may be left with significant morbidity including facial deformity, the loss of soft and hard tissue, scarring, xerostomia, mucositis, impaired articulation, impaired swallowing, and reduced social acceptability.1,7

While a reduced retention rate of implants is well documented in the literature,9–12 within our patient group, the 5 implant failures occurred only in irradiated bone that had been provided as part of a composite (soft tissue and bone) free flap. The bone in the free flap may not have been fully vascularized after transfer, resulting in poor osseointegration, or the bulky soft tissues may have led to peri-implantitis. There were no failures in irradiated jaw bone or bone grafts.

In an attempt to improve implant retention rates, and reduce the incidence of ORN, our patients underwent HBOT according to the Marx protocol.13 This protocol involves 20 treatments prior to placement of dental implants and 10 treatments subsequently at 2–2.5 ATA for 60 minutes.13

HBOT has been advocated to prevent ORN and improve implant retention.9,11,13 Clinicians want what is best for the patient, to avoid treatment failure and potential serious complications. However, HBOT is a laborious process for patients to endure. HBOT was used as a standard protocol for all 12 patients who had radiotherapy to the jaws in our patients, with the intention to reduce complications.

Hyperbaric oxygen treatment has so far in a randomized trial not shown to improve the survival of dental implants post radiotherapy.12 A Cochrane review by Esposito et al. in 2008 reported that HBOT may not provide any benefit to the success of implant prostheses in patients who have radiotherapy to the jaws.12 This view was solely based on a randomized controlled trial by Schoen, which met the inclusion criteria of the systematic review.14 Schoen’s paper showed no beneficial effect of HBOT with regard to implant survival and prevention of ORN when compared to patients who received only prophylactic antibiotics.12,14 Esposito’s review acknowledged that more clinical trials are needed, but a great ethical hurdle exists when it comes to designing randomized trials given the potentially severe side effect of ORN.14

Although Esposito’s review does not support the use of HBOT, the conclusion may not be that valuable as papers that advocated the use of HBO (notably by Granstrom et al.) were excluded.9,11 HBOT continues to be used in many cancer centres in Australia, and around the world where the facility is available, after radiotherapy prior to implant placement. The high retention rates seen in our patient group may have been due to HBOT in all of our patients.

It is estimated that the 31 patients selected in our cohort at the Royal Melbourne Hospital was approximately 2% of an approximate total of 1500 patients who underwent surgery for head and neck cancer at the Royal Melbourne Hospital during the study period. Patient selection is very important so that patients are not subjected to onerous treatment in the latter part of their lives, particularly if their prognosis is not favourable. Factors including age and medical comorbidities, such as diabetes, smoking, the use of steroid medication and radiotherapy are factors that can adversely affect the integration of dental implants.14 Patient motivation and commitment is also important to consider so that patients will complete treatment. These factors were considered by the Royal Melbourne Hospital Multidisciplinary team when selecting patients for dental implant based oral rehabilitation and would partially reflect the very low selection rate of oral cancer patients for dental implant placement. However, despite the selection criteria for implants provision, 3 patients were not able to tolerate wearing their oral prosthesis, and 5 patients died before provision of the final prosthesis. This reflects the challenge in providing dental implants based prosthesis in these patients.

In some cases, implants have been placed at the time of cancer resection and primary reconstruction. This saves the patient being subjected to implant surgery on a separate date. Implants placed at the time of surgery may be indicated where cancer surgery is limited to the soft tissue, or where resection of the oral cancer involves alveolar bone only.1 In cases where maxillectomy is performed, the implants may be placed into the zygoma. However, in larger resections it can be difficult to place the implants in a favourable position, particularly in combination with free flaps. In our experience, there can be significant soft tissue problems around the perforation of the oral mucosa. In addition, the patient’s long-term prognosis may not be clear (Fig 6).

image

Figure 6.  An unfortunate case of a 49-year-old woman who had primary placement of implant fixtures into iliac crest free flap and zygoma post orbito-maxillectomy at the time of primary surgery. The patient underwent postoperative radiotherapy and HBOT, and died one year after surgery due to disseminated disease, before a final orbito-maxillary prosthesis could be fitted.

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Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. References

Dental implants have an important role in the rehabilitation of oral cancer patients in the provision of an oral prosthesis. Healing and survival rates of implants may be influenced by the medical status of the patient, age and whether or not the patient has undergone radiotherapy.15 There was an increased risk of implant failure noted in free flap bone that had been irradiated within our patient cohort, however, this is not consistent with other reports in the literature.7,15

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. References
  • 1
    Marx RE, Morales MJ. The use of implants in the reconstruction of oral cancer patients. Dent Clin North Am 1998;42:117202.
  • 2
    Jham BC, Reis PM, Miranda EL, et al. Oral health status of 207 head and neck cancer patients before, during and after radiotherapy. Clin Oral Investig 2008;12:1924.
  • 3
    Rogers SN. Quality of life perspectives in patients with oral cancer. Oral Oncol 2010;46:445447.
  • 4
    English D, Farrugia H, Thursfield V, Chang P, Giles G. Cancer Survival Victoria 2007. Estimates of survival in 2004 (and comparisons with earlier periods). Melbourne: The Cancer Council Victoria Epidemiology Centre, 2007.
  • 5
    Brånemark PI, Lindström J, Hallén O, Breine U, Jeppson PH, Ohman A. Reconstruction of the defective mandible. Scand J Plast Reconstr Surg 1975;9:116128.
  • 6
    Brånemark PI, Breine U, Hallén O, Hanson B, Lindström J. Repair of defects in mandible. Scand J Plast Reconstr Surg 1970;4:100108.
  • 7
    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;67:24852496.
  • 8
    Brown JS, Magennis P, Rogers SN, Cawood JI, Howell R. Trends in head and neck microvascular reconstructive surgery in Liverpool (1992–2001). Br J Oral Maxillofac Surg 2006;44:364370.
  • 9
    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;57:493499.
  • 10
    Ihde S, Kopp S, Gundlach K, Konstantinović VS. Effects of radiation therapy on craniofacial and dental implants: a review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;107:5665.
  • 11
    Granström G. Placement of dental implants in irradiated bone: the case for using hyperbaric oxygen. J Oral Maxillofac Surg 2006;64:812818.
  • 12
    Esposito M, Grusovin MG, Patel S, Worthington HV, Coulthard P. Interventions for replacing missing teeth: hyperbaric oxygen therapy for irradiated patients who require dental implants. Cochrane Database Syst Rev 2008 Jan 23;(1):CD003603.
  • 13
    Marx RE, Johnson RP, Kline SN. Prevention of osteoradionecrosis: a randomized prospective clinical trial of hyperbaric oxygen versus penicillin. J Am Dent Assoc 1985;111:4954.
  • 14
    Schoen PJ, Raghoebar GM, Bouma J, 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;43:379388.
  • 15
    Moy PK, Medina D, Shetty V, Aghaloo TL. Dental implant failure rates and associated risk factors. Int J Oral Maxillofac Implants 2005;20:569577.