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Implant-Retained Dental Rehabilitation in Head and Neck Cancer Patients: An Assessment of Success and Failure Kanchan P. Dholam, MDS,* Hrishikesh A. Pusalkar, MDS,† Prabha S. Yadav, MS,‡ Ghazwan A. Quazi, MS,§ and Priyanka P. Somani, MDSk
blative surgery and reconstruction followed by radiation and/ or chemotherapy is the modality of treatment for head and neck cancers.1 After completion of treatment and control of disease, rehabilitation and restoration of function is a challenging task. Loss of vital structures and anatomical defects after surgery and reconstruction,2 effects of radiation on oral tissue, and missing dentition adversely affect oral rehabilitation.3 The presence of dentition is one of the main components for fabrication of a retentive and stable dental prosthesis, which will restore oral functions like mastication, swallowing, esthetics, and speech. Dental implants contribute to the feasibility of fabrication of implant-retained dental prostheses in head and neck cancer patients, facilitating restoration of oral functions. Implants can be placed in native bone or grafted bone according to the rehabilitation treatment plan.1,4,5
A
*Head and Professor, Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Mumbai, India. †Assistant Professor, Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Mumbai, India. ‡Head, Department of Cancer Surgery, Tata Memorial Hospital, Mumbai, India. §Assistant Professor, Department of Cancer Surgery, Tata Memorial Hospital, India. kFellow, Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Mumbai, India.
Reprint requests and correspondence to: K. P. Dholam, MDS, Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Dr. Ernest Borges Marg, Parel, Mumbai 400 012, India, Phone: +91-2224177224, Fax: +91-22-24146937, E-mail: kdholam@ hotmail.com ISSN 1056-6163/13/02206-604 Implant Dentistry Volume 22 Number 6 Copyright © 2013 by Lippincott Williams & Wilkins DOI: 10.1097/ID.0b013e3182a4d7bc
Background: This study aimed to evaluate the rate of osseointegration (ROI) and overall success rate (OSR) of implants placed in native and grafted jaws with or without radiotherapy at a 5-year follow-up in Indian head and neck cancer patients. Material and Methods: Thirty head and neck cancer patients from various socioeconomic strata were accrued. Eighty-five implants were inserted in 17 native and 13 grafted jaws. Nineteen patients received radiation therapy. A 5-year follow-up ROI and OSR of implants were reported. Results: The 5-year ROI and OSR were 88% and 77%, respectively. ROI
was 93% for grafted, 85% for native, 83% for irradiated, and 100% for nonirradiated jaws. OSR was 73% for grafted, 80% for native, 71% for irradiated, and 89% for nonirradiated jaws. Patients from higher socioeconomic strata had higher OSR (92%) as compared with those belonging to lower socioeconomic strata (65%). Conclusion: The failure rate observed in this study was 24% for implants placed in head and neck cancer patients at a 5-year followup. (Implant Dent 2013;22:604–609) Key Words: head and neck cancer, implants, irradiation, osseointegration, reconstruction
The success of implants depends on patient-related factors (age, diabetes, smoking), iatrogenic factors (overheating of bone during surgery, improper implant positioning), local factors (infection, quality and quantity of bone), and technical factors (implant type, size, surface characteristics, and prosthetic loading).6,7 In oral cancer patients, the effect of radiation therapy on vascular and cellular components of the tissues and altered anatomy due to reconstruction of the resected jaws are important determinants of osseointegration and overall success of implants.2,8,9 In addition to the above factors, which influence the success of implant-retained dental prostheses, the socioeconomic status with poor education background,
poor oral hygiene practice, and lack of compliance to postimplant rehabilitation care can also have significant influence on the final success. The purpose of this study was to evaluate the rate of osseointegration (ROI) and overall success rate (OSR) of implants placed in native and grafted jaws after ablative surgery, with or without radiation therapy at a 5-year follow-up in an Indian population.
MATERIAL
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METHODS
Thirty patients who were diagnosed and treated for tumor of the maxilla and mandible were accrued for the study. These patients underwent dental rehabilitation with implant-retained dental prosthesis from July 2003 to October 2008. The study was approved by the
IMPLANT DENTISTRY / VOLUME 22, NUMBER 6 2013 Tata Memorial Hospital Scientific and Ethics Review Committees. These patients were selected as per the following inclusion criteria: 1. Patients with resection of benign and malignant tumors of the jaw with or without radiotherapy and chemotherapy 2. Total and partial edentulous patients in need of dental rehabilitation and maxillary defects in edentulous patients needing obturators 3. Patients who were disease free for .1 year after completion of surgery, radiation and chemotherapy, and with good general condition 4. Patients of all socioeconomic strata 5. Patients without any other medical comorbidity 6. Patients who abstained from smoking and tobacco chewing after treatment for the disease. Microvascular free fibular graft reconstruction was either primary, that is, performed at the time of resection of the tumor, or secondary, that is, performed as a second procedure after resection.10 Implant placement if done at the time of reconstruction was considered primary and if done after reconstruction was considered secondary. Thirty patients were included in this study, 18 males and 12 females, with an age range of 13 to 82 years (average, 46 years) with varied histopathology (Tables 1 and 2). Eleven patients were not irradiated, whereas 19 patients received postoperative external beam radiation therapy with an average interval of 47 days between surgery and radiation. The range of the radiation dose was 20 to 60 Gy. The radiation dose was decided on the basis of histopathology report and stage of tumor (Table 2). These patients were considered for implant placement after completion of 1 year after radiotherapy. None of the patients received radiotherapy after implant placement. At our institute, patients from all over India register themselves according to their economic status. In our study, 12 patients were from high
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Table 1. Overview of the Study Sample selection No. of patients Mandible Maxilla Maxilla and mandible Male Female Age, y Radiated Nonradiated Radiation dose, Gy Diagnosis Squamous cell carcinoma Verrucous cell carcinoma Verrucous hyperplasia Epidermoid carcinoma Mucoepidermoid carcinoma Melanoma Fibroma Langerhans cell histiocytosis Chondroblastic osteogenic sarcoma Aneurysmal bone cyst Primary neoectodermal tumor Ameloblastoma Undifferentiated carcinoma Dental status Completely edentulous Partially edentulous Implants No. of implants No. of implants failed (%) Cause of failure Stages 1 and 2 After loading Prosthesis Over denture Fixed complete denture Fixed partial denture Obturator Bar-retained partial denture
socioeconomic status. Among them 10 patients had malignant lesions and only 2 were treated for benign lesion namely ameloblastoma. In the other 18 patients from low socioeconomic status, all the patients had malignant lesion except 3, that is, aneurysmal bone cyst, fibroma, and verrucous hyperplasia. A total of 85 dental implants were placed in the maxillary/mandibular anterior and premolar region. Thirteen patients had undergone reconstruction with microvascular free fibula graft in whom 40 dental implants were placed (Table 1). Primary reconstruction was
Native
Grafted
Total
17 13 2 2 11 6 14–82 11 6 20–60
13 11 2 0 7 6 13–56 8 5 50–60
30 24 4 2 18 12 13–82 (46) 19 11 20–60
11 1 1 1 0 1 1 1 0 0 0 0 0
4 2 0 0 1 0 0 0 1 1 1 2 1
15 3 1 1 1 1 1 1 1 1 1 2 1
12 5
7 6
19 11
45 9 (20)
40 11 (28)
85 20 (24)
7 2
3 8
10 10
10 0 2 2 0
4 2 1 0 1
14 2 3 2 1
done in 12 patients (11 mandible and 1 maxilla). This was decided by the surgical oncology team depending on the extent of the disease and when soft tissue reconstruction was not feasible. Of these, 2 patients had undergone maxillary reconstruction (1 primary reconstruction with secondary insertion of implants and 1 secondary reconstruction with primary insertion of implants). Secondary reconstruction of maxilla was done in case of primary neoectodermal tumor after 2 years of completion of treatment (surgery, radiotherapy, and chemotherapy) and disease-free state
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Table 2. Table Showing Histopathology, Staging, and Radiation Dose Tumor Type (Histopathology Report) Aneurysmal bone cyst Ameoloblastoma Chondroblastic osteogenic sarcoma Epidermoid carcinoma Fibroma Langerhans cell histiocytosis Melanoma Mucoepidermoid carcinoma PNET Squamous cell carcinoma
Undifferentiated carcinoma Verrucous cell carcinoma Verrucous hyperplasia
Tumor Stage
No. of Patients
Radiation Dose, Gy
Not applicable Not applicable Not known
1 2 1
Not applicable Not applicable Not applicable
Stage IV Not applicable Not known Not known Stage III Stage III Stage II Stage III Stage IV Unknown Unknown Stage III Stage IV Not applicable
1 1 1 1 1 1 1 6 6 2 1 1 2 1
Not applicable Not applicable 20 Not applicable 50 55 Not applicable 50–60 46–60 56 50 50 Not applicable Not applicable
for esthetic purpose. In this patient, primary implant placement during secondary reconstruction was done. Eleven patients who had mandibular continuity resection were primarily reconstructed with secondary insertion of implants (HiTec Implants, Ltd., Herzlia, Israel; and Herzalia 46722; LifeCare Devices, Mumbai, India). A total of 45 dental implants were placed in 17 patients with native jaws. Thirteen patients received implants in native mandible, 2 in native maxilla, and 2 patients were treated with implants in both maxilla and mandible. Eleven patients were partially edentulous, and 19 were completely edentulous (Table 1). Implants were loaded after 3 and 6 months in nonirradiated and irradiated patients, respectively, to allow the implants to osseointegrate. Clinical stability, absence of pain or infection, and radiographic evidence of osseointegration were considered the criteria for success. Second stage surgery was performed to uncover the implants, and periimplant mucosa was thinned. Healing caps were then attached to the implants. After 2 weeks, standard clinical and laboratory procedures were followed to fabricate implant-retained dental prosthesis. Patients were instructed and educated regarding the maintenance and cleaning of prosthesis, periimplant tissues, and oral health.
Clinical and radiological evaluation was done at a 6-month follow-up for 5 years examination using a standard protocol to assess ROI and OSR for implants. The implants were regularly assessed according to the criteria of Buser et al.11 These criteria comprise the absence of persistent complaints, such as pain or dysesthesia (this is limited to those patients who do not have existing paresthesia from tumor surgery), and the absence of repeated periimplant infection, fistula, or abscess. Furthermore, the mobility and radiolucency around the implant were assessed. ROI and OSR were compared between native and grafted jaws, irradiated and nonirradiated jaws, and patients belonging to high and low socioeconomic strata. Patients who received radiation was further categorized according to radiation dose into 3 groups namely ,50 Gy, 50 to 55 Gy, and .55 Gy. These patients were evaluated for ROI and OSR to assess the effect of radiation dosage on the success of implants. Statistical Analysis
Descriptive statistics is presented as average or proportion. Normality of data was assessed using the KolmogorovSmirnov test. Continuous variables were analyzed using the Mann-Whitney U test. Categorical variables were analyzed
ET AL
using the chi-square test. The KaplanMeier method was used to estimate the implant survival after placement. All the tests were conducted at 5% significance level. SPSS (Version 18) was used for data management.
RESULTS A total of 85 implants were placed in 30 patients. Forty-five implants were placed in 17 native jaws (11 irradiated and 6 nonirradiated) and 40 implants in 13 reconstructed jaws (8 irradiated and 5 nonirradiated). Fifty-nine implants were placed in 19 patients who received radiation therapy (range, 20–60 Gy) (Table 1). At a 5-year follow-up, 22 patients had functioning implant-retained dental prostheses. These included 3 fixed partial denture, 2 fixed complete denture, 14 over dentures, 2 definitive obturators, and 1 bar-retained dentures. These implant-retained dental prostheses were retained by 65 functioning implants. The ROI and OSR for implants was 88% and 77%, respectively. Ten implants failed after Stage I surgery, and 10 implants failed due to periimplantitis and bad positioning (3 implants) after loading. Five implants in native jaws were removed due to recurrence in 2 patients. Three patients died due to reasons beyond the scope of this project (2 patients died after Stage I and 1 after fabrication of obturator). The estimated survival free of failure at the end of 5 years was 75% (Table 3, Fig. 1). Sixty-five percent OSR was seen with 49 implants placed in 18 patients Table 3. Kaplan-Meier Estimates of Survival Free of Implant Failures Months After Implant Placement 0 12 24 36 48 60
No. of Implants Exposed to Risk
Cumulative Proportion Surviving at End of Interval
81.000 66.000 58.500 47.500 34.500 24.000
0.86 0.79 0.75 0.75 0.75 0.75
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failures (47%) were observed in patients who received 56 to 60 Gy of radiation dose.
DISCUSSION
Fig. 1. Kaplan-Meier curve of overall implant survival.
belonging to low socioeconomic strata. In these patients, 18 implant failures were observed. In the high socioeconomic strata, 92% OSR was observed with 36 implants placed in 12 patients. In native jaws, 80% OSR was observed, 7 implants failed after Stage I surgery (ROI, 85%) and 2 implants failed after prosthetic loading in irradiated patients. In grafted jaws, 73% OSR was observed 11 out of 40 implants failed in 4 patients. Three implants failures were observed after Stage I surgery (ROI, 93%) due to radiation therapy. Eight implants failed due to periimplantitis. Among these, in a nonirradiated patient, bad implant positioning was an additional cause of failure for 3 implants (Table 4). Seventy-one percent OSR of implants were seen in irradiated patients. Table 4. Showing ROI and OSR in Grafted and Native Jaws
ROI OSR
Native Jaws, %
Grafted Jaws, %
85 80
93 73
The cause of failure was lack of osseointegration (ROI, 83%) and periimplantitis. This was due to poor bone healing and soft tissue conditions due to the total irradiation dose delivered (.50 Gy). However, in nonirradiated jaws due to bad positioning and periimplantitis, 89% OSR of implants was seen. There was 100% success rate for osseointegration for implants in nonirradiated patients (Table 5). ROI and OSR of implants placed in patients with native and grafted jaws (P ¼ 0.465), irradiated and nonirradiated jaws (P ¼ 0.144), high and low socioeconomic strata (P ¼ 0.273) were not statistically significant. In the 3 groups of irradiated patients namely ,50 Gy, 50 to 55 Gy, and .55 Gy, there was a statistically significant difference in ROI and OSR. Maximum Table 5. Showing ROI and OSR in Irradiated and Nonirradiated Jaws
ROI OSR
Irradiated Jaws, %
Nonradiated Jaws, %
83 71
100 89
The success of osseointegration of implants in patients having undergone oral cancer therapy remains unclear. Surgical excision of oral malignancies is often followed by radiotherapy, chemotherapy, or both. Irradiated sites are more susceptible to tissue necrosis and consequent loss of implants compared with nonirradiated sites. In the study by Schoen et al,12 prognosis of implant-retained dental prostheses was shown to be superior in nonirradiated patients compared with irradiated patients after oral cancer surgery. Studies by Kovács13,14 conclude that implants can successfully osseointegrate where patients have undergone chemotherapy provided that implants are inserted after 6 months of chemotherapy. Yi-Qun et al15 placed 29 implants in maxillae and 88 in mandibles. Seventeen implants were placed in native jaws and 100 implants in fibula bone flaps. The 1-year and 5-year cumulative success rates of implants placed in fibula bone grafts were 95% and 87%, respectively. The main reasons for failure of implants were infection, tumor recurrence, and soft tissue proliferation. Six patients (17 implants) who had soft tissue hyperplasia needed surgical removal of implants. Beumer et al16 reported success rates for implants in radiated bone sites between 60% and 69% for implants placed between 1985 and 1994. Betz et al17 have an OSR of 78%. Out of 59 tumor patients, treated from 1988 to 1996 with 261 implants, 23 patients with 99 implants were provided with dentures. A total of 68 out of 99 implants were inserted into autologous reconstructed mandible. Tumor patients had significantly worse periimplant parameter than nontumor patients. Toeh et al18 report survival rates of 97.0%, 97%, and 80% at 1, 5, and 10 years follow-up, respectively. The success was compromised by comorbidities like radiotherapy, lack of patient cooperation, or poor oral hygiene. Periimplant conditions and thickness and mobility of soft tissues
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were causes of late implant failure. The overall incidence of periimplantitis inflammation (including mucositis and periimplantitis) was reported to be 38%.19 Urken et al10 in their series of 210 mandibular reconstructions showed that 202 were successful in reestablishing mandibular continuity. The OSR for implants was 92%. The implants success rate was 86%, when the bone in which the fixtures were placed was irradiated postoperatively. The success rate was 64% in the 14 fixtures that were placed into previously irradiated bone. In the study by Anne-Gaëlle et al20 at 5 years, ROI and OSR for all implants was 91% and 78%, respectively. The cause of failure was radiation and periimplantitis and bad positioning of implants. The ROI and OSR seen in this study are comparable to the results reported by Beumer et al16 (OSR, 68%), Betz et al17 (OSR, 78%), and Anne-Gaëlle et al20 (ROI, 91% and OSR, 78%). The OSR in this study is less as compared with the results published by Yi-Qun et al15 (87%), Toeh et al18 (97%), and Urken et al10 (92%). Overall estimated implant survival free of failure at 5 years was 75%, which is lesser than that reported by Buddula et al1 (90%). In this clinical report, 71% OSR is observed at 5 years for implants placed in irradiated bone. Similar trends of OSR are observed by Urken et al10 (64%) and Beumer et al16 (61%). The OSR in nonirradiated jaws is higher than in irradiated jaws as stated by Beumer et al16 (76%) and Urken et al10 (92%). This is similar to OSR seen in this study. Maximum implant failures were seen for radiation doses 56 to 60 Gy. Health has been defined not simply as a state free from disease but as “the capacity of people to adapt to, respond to, or control life’s challenges and changes.”21 Profound differences in overall health status exist between developed and developing nations. Much of this has to do with the lack of the basic necessities of life (food, education, culture, facilities of living environment, sanitation, and health care). In this study on Indian population, the
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socioeconomic factor played a dominating role in the OSR of implants. Sixtyfive percent OSR was seen in patients belonging to low socioeconomic strata. Ninety-two percent OSR was observed in high socioeconomic strata which is comparable to the results reported by Yi-Qun et al15 (87%), Toeh et al18 (97%), and Urken et al10 (92%). In India, the lower socioeconomic subjects are with poor education background. Therefore, they were not able to follow and pursue the instructions on maintenance and cleaning of the tissues and prosthesis and thus achieve a good level of oral hygiene. Hence, in this study, it was observed that in Indian head and neck cancer patients, radiation therapy and low socioeconomic strata lead to a lack of osseointegration and periimplantitis, which results in the failure of implants. Despite the optimal instructions given to the patients and reinforcement of the same, periimplantitis persisted that leads to clinical or absolute failure.22 It was observed more with fixed prostheses as compared with removable prostheses. This could be attributed to the lapse on the part of the patient to pursue and follow oral hygiene instructions,20 lack of attached mucosa, and altered anatomy and histology in reconstructed jaws.19,20 Malpositioning is another cause that can lead to implant and prosthesis failure in this subset of patients. Reconstruction after resection surgery in head and neck cancer patients also affected implant success.
CONCLUSIONS Radiotherapy, in head and neck cancer patients, is one of the main factors affecting the osseointegration of dental implants. Altered tissue histology and soft tissue thickness subsequent to reconstruction along with radiotherapy are contributing factors for periimplantitis. Lack of motivation for maintenance of oral hygiene, unavailability of resources, and facilities amongst the low socioeconomic strata lead to periimplantitis, which also has a significant effect on the success rate of dental implants in Indian head and neck cancer patients. The failure rate observed in this study is 24% for implants placed in
ET AL
head and neck cancer patients at a 5year follow-up.
DISCLOSURE The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.
ACKNOWLEDGMENTS This work was supported by Tata Memorial Hospital Intramural Funds (Project No. 132 to K.P.D.).
REFERENCES 1. Buddula A, Assad DA, Salinas TJ, et al. Survival of dental implants in irradiated head and neck cancer patients: A retrospective analysis. Clin Implant Dent Relat Res. 2012;14:716–722. doi:10.1111/j. 1708-8208.2010.00307. 2. 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: 493–499. 3. Meraw SJ, Reeve CM. Dental considerations and treatment of the oncology patients receiving radiation therapy. J Am Dent Assoc. 1998;129:201–205. 4. Disa JJ, Cordeiro PG. Mandible reconstruction with microvascular surgery. Semin Surg Oncol. 2000;19:226–234. 5. Sumi Y, Hasegawa T, Miyaishi O, et al. Interface analysis of titanium implants in a human vascularized fibula bone graft. J Oral Maxillofac Surg. 2001;59:213–216. 6. Wu PBC, Yung WCW. Factors contributing to implant failure. Hong Kong Dental J. 2005;2:12–18. 7. Misch CE. Contemporary Implant Dentistry. 3rd ed. St Louis, MO: Mosby; 2007. 8. 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;69:60–69. 9. Larsen PE, Stronczek MJ, Beck FM, et al. Osteointegration of implants in radiated bone with and without adjunctive hyperbaric oxygen. J Oral Maxillofac Surg. 1993;51:280–287. 10. Urken ML, Buchbinder D, Costantino PD, et al. Oromandibular reconstruction using microvascular composite flaps: Report of 210 cases. Arch Otolaryngol Head Neck Surg. 1998;124: 46–55.
IMPLANT DENTISTRY / VOLUME 22, NUMBER 6 2013 11. Buser D, Ingimarsson S, Dula K, et al. Long-term stability of osseointegrated implants in augmented bone: A 5-year prospective study in partially edentulous patients. Int J Periodontics Restorative Dent. 2002;22:109–117. 12. Schoen PJ, Raghoebar GM, Bouma J, et al. Prosthodontic rehabilitation of oral function in head–neck cancer patients with dental implants placed simultaneously during ablative tumor surgery: An assessment of treatment outcomes and quality of life. Int J Oral Maxillofac Surg. 2008;37:8–16. 13. Kovács AF. Influence of chemotherapy on endosteal implant survival and success in oral cancer patients. Int J Oral Maxillofac Surg. 2001;30:144–147. 14. Kovács AF. The fate of osseointegrated implants in patients following oral cancer surgery and mandibular reconstruction. Head Neck. 2000;22:111–119.
15. Yi-Qun W, Wei H, Zhi-Yong Z, et al. Clinical outcome of dental implants placed in fibula-free flaps for orofacial reconstruction. Chin Med J. 2008;121:1861–1865. 16. Beumer J III, Roumanas E, Nishimura R. Advances in osseointegrated implants for dental and facial rehabilitation following major head and neck surgery. Semin Surg Oncol. 1995;11:200–207. 17. Betz T, Purps S, Pistner H, et al. Oral rehabilitation of tumor patients with endosseous implants. Implant success with special reference to peri-implant tissue [in German]. Mund Kiefer Gesichtschir. 1999;3(suppl 1):S99–S105. 18. Toeh K, Huryn J, Patel S, et al. Implant prosthodontic rehabilitation of fibula free flaps reconstructed mandibles: A Sloan Memorial Kettering Cancer Centre review of prognosis factor and implant outcomes. Int J Oral Maxillofac Implants. 2005;20:738–746.
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19. Blake F, Bubenheim M, Heiland M, et al. Retrospective assessment of the peri-implant mucosa of implants inserted in reanastomosed or free bone grafts from the fibula or iliac crest. Int J Oral Maxillofac Implants. 2008;23:1102–1108. 20. Anne-Gaëlle B, Samuel S, Julie B, et al. Dental implant placement after mandibular reconstruction by microvascular free fibula flap: Current knowledge and remaining questions. Oral Oncol. 2011;47:1099–1104. 21. Frankish CJ. Health Impact Assessment as a Tool for Population Health Promotion and Public Policy. Vancouver, Canada: Institute of Health Promotion Research, University of British Columbia; 1996. 22. Misch CE, Perel ML, Wang HL, et al. Implant success, survival, and failure: The International Congress of Oral Implantologists (ICOI) Pisa Consensus Conference. Implant Dent. 2008;17:5–15.
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Implant-Retained Dental Rehabilitation in Head and Neck Cancer Patients: An Assessment of Success and Failure Kanchan P. Dholam, MDS,* Hrishikesh A. Pusalkar, MDS,† Prabha S. Yadav, MS,‡ Ghazwan A. Quazi, MS,§ and Priyanka P. Somani, MDSk
blative surgery and reconstruction followed by radiation and/ or chemotherapy is the modality of treatment for head and neck cancers.1 After completion of treatment and control of disease, rehabilitation and restoration of function is a challenging task. Loss of vital structures and anatomical defects after surgery and reconstruction,2 effects of radiation on oral tissue, and missing dentition adversely affect oral rehabilitation.3 The presence of dentition is one of the main components for fabrication of a retentive and stable dental prosthesis, which will restore oral functions like mastication, swallowing, esthetics, and speech. Dental implants contribute to the feasibility of fabrication of implant-retained dental prostheses in head and neck cancer patients, facilitating restoration of oral functions. Implants can be placed in native bone or grafted bone according to the rehabilitation treatment plan.1,4,5
A
*Head and Professor, Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Mumbai, India. †Assistant Professor, Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Mumbai, India. ‡Head, Department of Cancer Surgery, Tata Memorial Hospital, Mumbai, India. §Assistant Professor, Department of Cancer Surgery, Tata Memorial Hospital, India. kFellow, Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Mumbai, India.
Reprint requests and correspondence to: K. P. Dholam, MDS, Department of Dental and Prosthetic Surgery, Tata Memorial Hospital, Dr. Ernest Borges Marg, Parel, Mumbai 400 012, India, Phone: +91-2224177224, Fax: +91-22-24146937, E-mail: kdholam@ hotmail.com ISSN 1056-6163/13/02206-604 Implant Dentistry Volume 22 Number 6 Copyright © 2013 by Lippincott Williams & Wilkins DOI: 10.1097/ID.0b013e3182a4d7bc
Background: This study aimed to evaluate the rate of osseointegration (ROI) and overall success rate (OSR) of implants placed in native and grafted jaws with or without radiotherapy at a 5-year follow-up in Indian head and neck cancer patients. Material and Methods: Thirty head and neck cancer patients from various socioeconomic strata were accrued. Eighty-five implants were inserted in 17 native and 13 grafted jaws. Nineteen patients received radiation therapy. A 5-year follow-up ROI and OSR of implants were reported. Results: The 5-year ROI and OSR were 88% and 77%, respectively. ROI
was 93% for grafted, 85% for native, 83% for irradiated, and 100% for nonirradiated jaws. OSR was 73% for grafted, 80% for native, 71% for irradiated, and 89% for nonirradiated jaws. Patients from higher socioeconomic strata had higher OSR (92%) as compared with those belonging to lower socioeconomic strata (65%). Conclusion: The failure rate observed in this study was 24% for implants placed in head and neck cancer patients at a 5-year followup. (Implant Dent 2013;22:604–609) Key Words: head and neck cancer, implants, irradiation, osseointegration, reconstruction
The success of implants depends on patient-related factors (age, diabetes, smoking), iatrogenic factors (overheating of bone during surgery, improper implant positioning), local factors (infection, quality and quantity of bone), and technical factors (implant type, size, surface characteristics, and prosthetic loading).6,7 In oral cancer patients, the effect of radiation therapy on vascular and cellular components of the tissues and altered anatomy due to reconstruction of the resected jaws are important determinants of osseointegration and overall success of implants.2,8,9 In addition to the above factors, which influence the success of implant-retained dental prostheses, the socioeconomic status with poor education background,
poor oral hygiene practice, and lack of compliance to postimplant rehabilitation care can also have significant influence on the final success. The purpose of this study was to evaluate the rate of osseointegration (ROI) and overall success rate (OSR) of implants placed in native and grafted jaws after ablative surgery, with or without radiation therapy at a 5-year follow-up in an Indian population.
MATERIAL
AND
METHODS
Thirty patients who were diagnosed and treated for tumor of the maxilla and mandible were accrued for the study. These patients underwent dental rehabilitation with implant-retained dental prosthesis from July 2003 to October 2008. The study was approved by the
IMPLANT DENTISTRY / VOLUME 22, NUMBER 6 2013 Tata Memorial Hospital Scientific and Ethics Review Committees. These patients were selected as per the following inclusion criteria: 1. Patients with resection of benign and malignant tumors of the jaw with or without radiotherapy and chemotherapy 2. Total and partial edentulous patients in need of dental rehabilitation and maxillary defects in edentulous patients needing obturators 3. Patients who were disease free for .1 year after completion of surgery, radiation and chemotherapy, and with good general condition 4. Patients of all socioeconomic strata 5. Patients without any other medical comorbidity 6. Patients who abstained from smoking and tobacco chewing after treatment for the disease. Microvascular free fibular graft reconstruction was either primary, that is, performed at the time of resection of the tumor, or secondary, that is, performed as a second procedure after resection.10 Implant placement if done at the time of reconstruction was considered primary and if done after reconstruction was considered secondary. Thirty patients were included in this study, 18 males and 12 females, with an age range of 13 to 82 years (average, 46 years) with varied histopathology (Tables 1 and 2). Eleven patients were not irradiated, whereas 19 patients received postoperative external beam radiation therapy with an average interval of 47 days between surgery and radiation. The range of the radiation dose was 20 to 60 Gy. The radiation dose was decided on the basis of histopathology report and stage of tumor (Table 2). These patients were considered for implant placement after completion of 1 year after radiotherapy. None of the patients received radiotherapy after implant placement. At our institute, patients from all over India register themselves according to their economic status. In our study, 12 patients were from high
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Table 1. Overview of the Study Sample selection No. of patients Mandible Maxilla Maxilla and mandible Male Female Age, y Radiated Nonradiated Radiation dose, Gy Diagnosis Squamous cell carcinoma Verrucous cell carcinoma Verrucous hyperplasia Epidermoid carcinoma Mucoepidermoid carcinoma Melanoma Fibroma Langerhans cell histiocytosis Chondroblastic osteogenic sarcoma Aneurysmal bone cyst Primary neoectodermal tumor Ameloblastoma Undifferentiated carcinoma Dental status Completely edentulous Partially edentulous Implants No. of implants No. of implants failed (%) Cause of failure Stages 1 and 2 After loading Prosthesis Over denture Fixed complete denture Fixed partial denture Obturator Bar-retained partial denture
socioeconomic status. Among them 10 patients had malignant lesions and only 2 were treated for benign lesion namely ameloblastoma. In the other 18 patients from low socioeconomic status, all the patients had malignant lesion except 3, that is, aneurysmal bone cyst, fibroma, and verrucous hyperplasia. A total of 85 dental implants were placed in the maxillary/mandibular anterior and premolar region. Thirteen patients had undergone reconstruction with microvascular free fibula graft in whom 40 dental implants were placed (Table 1). Primary reconstruction was
Native
Grafted
Total
17 13 2 2 11 6 14–82 11 6 20–60
13 11 2 0 7 6 13–56 8 5 50–60
30 24 4 2 18 12 13–82 (46) 19 11 20–60
11 1 1 1 0 1 1 1 0 0 0 0 0
4 2 0 0 1 0 0 0 1 1 1 2 1
15 3 1 1 1 1 1 1 1 1 1 2 1
12 5
7 6
19 11
45 9 (20)
40 11 (28)
85 20 (24)
7 2
3 8
10 10
10 0 2 2 0
4 2 1 0 1
14 2 3 2 1
done in 12 patients (11 mandible and 1 maxilla). This was decided by the surgical oncology team depending on the extent of the disease and when soft tissue reconstruction was not feasible. Of these, 2 patients had undergone maxillary reconstruction (1 primary reconstruction with secondary insertion of implants and 1 secondary reconstruction with primary insertion of implants). Secondary reconstruction of maxilla was done in case of primary neoectodermal tumor after 2 years of completion of treatment (surgery, radiotherapy, and chemotherapy) and disease-free state
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Table 2. Table Showing Histopathology, Staging, and Radiation Dose Tumor Type (Histopathology Report) Aneurysmal bone cyst Ameoloblastoma Chondroblastic osteogenic sarcoma Epidermoid carcinoma Fibroma Langerhans cell histiocytosis Melanoma Mucoepidermoid carcinoma PNET Squamous cell carcinoma
Undifferentiated carcinoma Verrucous cell carcinoma Verrucous hyperplasia
Tumor Stage
No. of Patients
Radiation Dose, Gy
Not applicable Not applicable Not known
1 2 1
Not applicable Not applicable Not applicable
Stage IV Not applicable Not known Not known Stage III Stage III Stage II Stage III Stage IV Unknown Unknown Stage III Stage IV Not applicable
1 1 1 1 1 1 1 6 6 2 1 1 2 1
Not applicable Not applicable 20 Not applicable 50 55 Not applicable 50–60 46–60 56 50 50 Not applicable Not applicable
for esthetic purpose. In this patient, primary implant placement during secondary reconstruction was done. Eleven patients who had mandibular continuity resection were primarily reconstructed with secondary insertion of implants (HiTec Implants, Ltd., Herzlia, Israel; and Herzalia 46722; LifeCare Devices, Mumbai, India). A total of 45 dental implants were placed in 17 patients with native jaws. Thirteen patients received implants in native mandible, 2 in native maxilla, and 2 patients were treated with implants in both maxilla and mandible. Eleven patients were partially edentulous, and 19 were completely edentulous (Table 1). Implants were loaded after 3 and 6 months in nonirradiated and irradiated patients, respectively, to allow the implants to osseointegrate. Clinical stability, absence of pain or infection, and radiographic evidence of osseointegration were considered the criteria for success. Second stage surgery was performed to uncover the implants, and periimplant mucosa was thinned. Healing caps were then attached to the implants. After 2 weeks, standard clinical and laboratory procedures were followed to fabricate implant-retained dental prosthesis. Patients were instructed and educated regarding the maintenance and cleaning of prosthesis, periimplant tissues, and oral health.
Clinical and radiological evaluation was done at a 6-month follow-up for 5 years examination using a standard protocol to assess ROI and OSR for implants. The implants were regularly assessed according to the criteria of Buser et al.11 These criteria comprise the absence of persistent complaints, such as pain or dysesthesia (this is limited to those patients who do not have existing paresthesia from tumor surgery), and the absence of repeated periimplant infection, fistula, or abscess. Furthermore, the mobility and radiolucency around the implant were assessed. ROI and OSR were compared between native and grafted jaws, irradiated and nonirradiated jaws, and patients belonging to high and low socioeconomic strata. Patients who received radiation was further categorized according to radiation dose into 3 groups namely ,50 Gy, 50 to 55 Gy, and .55 Gy. These patients were evaluated for ROI and OSR to assess the effect of radiation dosage on the success of implants. Statistical Analysis
Descriptive statistics is presented as average or proportion. Normality of data was assessed using the KolmogorovSmirnov test. Continuous variables were analyzed using the Mann-Whitney U test. Categorical variables were analyzed
ET AL
using the chi-square test. The KaplanMeier method was used to estimate the implant survival after placement. All the tests were conducted at 5% significance level. SPSS (Version 18) was used for data management.
RESULTS A total of 85 implants were placed in 30 patients. Forty-five implants were placed in 17 native jaws (11 irradiated and 6 nonirradiated) and 40 implants in 13 reconstructed jaws (8 irradiated and 5 nonirradiated). Fifty-nine implants were placed in 19 patients who received radiation therapy (range, 20–60 Gy) (Table 1). At a 5-year follow-up, 22 patients had functioning implant-retained dental prostheses. These included 3 fixed partial denture, 2 fixed complete denture, 14 over dentures, 2 definitive obturators, and 1 bar-retained dentures. These implant-retained dental prostheses were retained by 65 functioning implants. The ROI and OSR for implants was 88% and 77%, respectively. Ten implants failed after Stage I surgery, and 10 implants failed due to periimplantitis and bad positioning (3 implants) after loading. Five implants in native jaws were removed due to recurrence in 2 patients. Three patients died due to reasons beyond the scope of this project (2 patients died after Stage I and 1 after fabrication of obturator). The estimated survival free of failure at the end of 5 years was 75% (Table 3, Fig. 1). Sixty-five percent OSR was seen with 49 implants placed in 18 patients Table 3. Kaplan-Meier Estimates of Survival Free of Implant Failures Months After Implant Placement 0 12 24 36 48 60
No. of Implants Exposed to Risk
Cumulative Proportion Surviving at End of Interval
81.000 66.000 58.500 47.500 34.500 24.000
0.86 0.79 0.75 0.75 0.75 0.75
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failures (47%) were observed in patients who received 56 to 60 Gy of radiation dose.
DISCUSSION
Fig. 1. Kaplan-Meier curve of overall implant survival.
belonging to low socioeconomic strata. In these patients, 18 implant failures were observed. In the high socioeconomic strata, 92% OSR was observed with 36 implants placed in 12 patients. In native jaws, 80% OSR was observed, 7 implants failed after Stage I surgery (ROI, 85%) and 2 implants failed after prosthetic loading in irradiated patients. In grafted jaws, 73% OSR was observed 11 out of 40 implants failed in 4 patients. Three implants failures were observed after Stage I surgery (ROI, 93%) due to radiation therapy. Eight implants failed due to periimplantitis. Among these, in a nonirradiated patient, bad implant positioning was an additional cause of failure for 3 implants (Table 4). Seventy-one percent OSR of implants were seen in irradiated patients. Table 4. Showing ROI and OSR in Grafted and Native Jaws
ROI OSR
Native Jaws, %
Grafted Jaws, %
85 80
93 73
The cause of failure was lack of osseointegration (ROI, 83%) and periimplantitis. This was due to poor bone healing and soft tissue conditions due to the total irradiation dose delivered (.50 Gy). However, in nonirradiated jaws due to bad positioning and periimplantitis, 89% OSR of implants was seen. There was 100% success rate for osseointegration for implants in nonirradiated patients (Table 5). ROI and OSR of implants placed in patients with native and grafted jaws (P ¼ 0.465), irradiated and nonirradiated jaws (P ¼ 0.144), high and low socioeconomic strata (P ¼ 0.273) were not statistically significant. In the 3 groups of irradiated patients namely ,50 Gy, 50 to 55 Gy, and .55 Gy, there was a statistically significant difference in ROI and OSR. Maximum Table 5. Showing ROI and OSR in Irradiated and Nonirradiated Jaws
ROI OSR
Irradiated Jaws, %
Nonradiated Jaws, %
83 71
100 89
The success of osseointegration of implants in patients having undergone oral cancer therapy remains unclear. Surgical excision of oral malignancies is often followed by radiotherapy, chemotherapy, or both. Irradiated sites are more susceptible to tissue necrosis and consequent loss of implants compared with nonirradiated sites. In the study by Schoen et al,12 prognosis of implant-retained dental prostheses was shown to be superior in nonirradiated patients compared with irradiated patients after oral cancer surgery. Studies by Kovács13,14 conclude that implants can successfully osseointegrate where patients have undergone chemotherapy provided that implants are inserted after 6 months of chemotherapy. Yi-Qun et al15 placed 29 implants in maxillae and 88 in mandibles. Seventeen implants were placed in native jaws and 100 implants in fibula bone flaps. The 1-year and 5-year cumulative success rates of implants placed in fibula bone grafts were 95% and 87%, respectively. The main reasons for failure of implants were infection, tumor recurrence, and soft tissue proliferation. Six patients (17 implants) who had soft tissue hyperplasia needed surgical removal of implants. Beumer et al16 reported success rates for implants in radiated bone sites between 60% and 69% for implants placed between 1985 and 1994. Betz et al17 have an OSR of 78%. Out of 59 tumor patients, treated from 1988 to 1996 with 261 implants, 23 patients with 99 implants were provided with dentures. A total of 68 out of 99 implants were inserted into autologous reconstructed mandible. Tumor patients had significantly worse periimplant parameter than nontumor patients. Toeh et al18 report survival rates of 97.0%, 97%, and 80% at 1, 5, and 10 years follow-up, respectively. The success was compromised by comorbidities like radiotherapy, lack of patient cooperation, or poor oral hygiene. Periimplant conditions and thickness and mobility of soft tissues
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were causes of late implant failure. The overall incidence of periimplantitis inflammation (including mucositis and periimplantitis) was reported to be 38%.19 Urken et al10 in their series of 210 mandibular reconstructions showed that 202 were successful in reestablishing mandibular continuity. The OSR for implants was 92%. The implants success rate was 86%, when the bone in which the fixtures were placed was irradiated postoperatively. The success rate was 64% in the 14 fixtures that were placed into previously irradiated bone. In the study by Anne-Gaëlle et al20 at 5 years, ROI and OSR for all implants was 91% and 78%, respectively. The cause of failure was radiation and periimplantitis and bad positioning of implants. The ROI and OSR seen in this study are comparable to the results reported by Beumer et al16 (OSR, 68%), Betz et al17 (OSR, 78%), and Anne-Gaëlle et al20 (ROI, 91% and OSR, 78%). The OSR in this study is less as compared with the results published by Yi-Qun et al15 (87%), Toeh et al18 (97%), and Urken et al10 (92%). Overall estimated implant survival free of failure at 5 years was 75%, which is lesser than that reported by Buddula et al1 (90%). In this clinical report, 71% OSR is observed at 5 years for implants placed in irradiated bone. Similar trends of OSR are observed by Urken et al10 (64%) and Beumer et al16 (61%). The OSR in nonirradiated jaws is higher than in irradiated jaws as stated by Beumer et al16 (76%) and Urken et al10 (92%). This is similar to OSR seen in this study. Maximum implant failures were seen for radiation doses 56 to 60 Gy. Health has been defined not simply as a state free from disease but as “the capacity of people to adapt to, respond to, or control life’s challenges and changes.”21 Profound differences in overall health status exist between developed and developing nations. Much of this has to do with the lack of the basic necessities of life (food, education, culture, facilities of living environment, sanitation, and health care). In this study on Indian population, the
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socioeconomic factor played a dominating role in the OSR of implants. Sixtyfive percent OSR was seen in patients belonging to low socioeconomic strata. Ninety-two percent OSR was observed in high socioeconomic strata which is comparable to the results reported by Yi-Qun et al15 (87%), Toeh et al18 (97%), and Urken et al10 (92%). In India, the lower socioeconomic subjects are with poor education background. Therefore, they were not able to follow and pursue the instructions on maintenance and cleaning of the tissues and prosthesis and thus achieve a good level of oral hygiene. Hence, in this study, it was observed that in Indian head and neck cancer patients, radiation therapy and low socioeconomic strata lead to a lack of osseointegration and periimplantitis, which results in the failure of implants. Despite the optimal instructions given to the patients and reinforcement of the same, periimplantitis persisted that leads to clinical or absolute failure.22 It was observed more with fixed prostheses as compared with removable prostheses. This could be attributed to the lapse on the part of the patient to pursue and follow oral hygiene instructions,20 lack of attached mucosa, and altered anatomy and histology in reconstructed jaws.19,20 Malpositioning is another cause that can lead to implant and prosthesis failure in this subset of patients. Reconstruction after resection surgery in head and neck cancer patients also affected implant success.
CONCLUSIONS Radiotherapy, in head and neck cancer patients, is one of the main factors affecting the osseointegration of dental implants. Altered tissue histology and soft tissue thickness subsequent to reconstruction along with radiotherapy are contributing factors for periimplantitis. Lack of motivation for maintenance of oral hygiene, unavailability of resources, and facilities amongst the low socioeconomic strata lead to periimplantitis, which also has a significant effect on the success rate of dental implants in Indian head and neck cancer patients. The failure rate observed in this study is 24% for implants placed in
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head and neck cancer patients at a 5year follow-up.
DISCLOSURE The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.
ACKNOWLEDGMENTS This work was supported by Tata Memorial Hospital Intramural Funds (Project No. 132 to K.P.D.).
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19. Blake F, Bubenheim M, Heiland M, et al. Retrospective assessment of the peri-implant mucosa of implants inserted in reanastomosed or free bone grafts from the fibula or iliac crest. Int J Oral Maxillofac Implants. 2008;23:1102–1108. 20. Anne-Gaëlle B, Samuel S, Julie B, et al. Dental implant placement after mandibular reconstruction by microvascular free fibula flap: Current knowledge and remaining questions. Oral Oncol. 2011;47:1099–1104. 21. Frankish CJ. Health Impact Assessment as a Tool for Population Health Promotion and Public Policy. Vancouver, Canada: Institute of Health Promotion Research, University of British Columbia; 1996. 22. Misch CE, Perel ML, Wang HL, et al. Implant success, survival, and failure: The International Congress of Oral Implantologists (ICOI) Pisa Consensus Conference. Implant Dent. 2008;17:5–15.
