Factors affecting the survival of implants placed in grafted maxillary sinuses: A clinical report
Joseph Y. K. Kan, DDS, MS,a Kitichai Rungcharassaeng, DDS, MS,b Jay Kim, PhD,c Jaime L. Lozada, DDS,d and Charles J. Goodacre, DDS, MSDe School of Dentistry, Loma Linda University, Loma Linda, Calif.
Many factors affect the survival rate of osseointegrated implants placed in grafted maxillary sinuses. This clinical report describes the retrospective evaluation of 60 patients with 228 implants placed in 84 grafted maxillary sinuses at the Loma Linda University School of Dentistry. The factors used to determine the survival rates of these implants were implant type, simultaneous/delayed implant placement, pretreatment bone height, oral hygiene, and cigarette smoking habits. Out of the total 228 implants, 205 (89.9%) remained in function after a mean follow-up period of 41.6 months (range 0 to 60 months). A higher failure rate was associated with the use of non-threaded implants, poor oral hygiene, and smoking. This information may facilitate treatment planning and enhance communication between the dentist and patient regarding the risk/benefit ratio and outcomes of implants placed in grafted maxillary sinuses.
(J Prosthet Dent 2002;87:485-9.)
Poor bone quality and quantity, in addition to anatomic variations, often are encountered during implant placement in the posterior maxilla. Maxillary
posterior bone atrophy together with pneumatization of the maxillary sinus following loss of dentition can prevent the placement of implants of optimal length.
Implant failure rates as high as 35% have been reported in type IV bone, which commonly is found in the posterior maxilla.1-3 In 1980 Boyne and James4 advocated placement of autogenous marrow and cancellous bone from the iliac crest into the pneumatized maxillary sinus to increase the amount of bone available for implant placement. Since then, numerous surgical techniques and graft materials have been suggested for this procedure.5-10 The reported results have been favorable and comparable to implants placed in adjacent non-grafted sites, regardless of the techniques and graft materials used.7,11-15
Insufficient and conflicting data have been reported relative to the effect of the following factors on implant success: implant type, implant placement simultaneous with or subsequent to maxillary sinus grafting, pretreatment bone height, oral hygiene status, and patient history of cigarette smoking. Some researchers and clinicians have suggested that both implant geometry and surface affect primary implant stability and therefore implant success and/or sur-vival.16-18 Brunski16 reported that screw-shaped implants provided the strongest retention immediately after implant placement. Others reported comparable success and/or survival rates for threaded implants12,19,20 and non-threaded implants.9,10,21
Although implants with coated surfaces have been shown to increase the rate and magnitude of osseous adaptation,17,18,22 the coating has not been shown to foster higher implant success or survival rates.
Whether implants should be placed simultaneously with or subsequent to maxillary sinus grafting is a matter of debate.10-12,15 The advantages of simultaneous implant placement are that this protocol minimizes the cost and number of surgical procedures and that loading can be initiated earlier and therefore enhance graft preservation.10,12,15
However, the delayed approach allows time for graft maturation and may provide more predictability, especially when the residual ridge is insufficient for initial implant stability.11,15 Moreover, delayed placement may foster implant placement in more ideal positions and angulations.11,15
It has been suggested that pretreatment bone height affects initial implant stability and therefore ultimate implant success.6,11,23 This variable also influences the clinician’s choice of implant type and graft materials, and it has been considered a prognosticator of whether implants should be placed simultaneous with or subsequent to sinus grafting.15 A minimum of 4- to 5-mm pretreatment bone height has been recommended for simultaneous implant placement.6,23
The influence of oral hygiene on implant success has been controversial.24-30 Although it is generally agreed that plaque accumulation may induce a negative mucosal response,24,25 Smith and Zarb26 argued that peri-implant mucosal response should not be a criterion for implant success because it has not been
MAY 2002 THE JOURNAL OF PROSTHETIC DENTISTRY 485
Table I. Summary of patient selection
Patients who completed surgical and prosthodontic phases at LLUSD – 72
Patients who could not be contacted due to change
of phone number or address – 9
Patients who declined to participate due to health problem – 1
Patients who declined to participate due to inconveniences in transportation – 1
Patients who died – 1
Total patients included in the study – 60
Table II. Success criteria* for osseointegrated implants proposed by Smith and Zarb 22
1. The individual unattached implant is immobile when tested clinically.
2. No evidence of peri-implant radiolucency is present as
assessed on an undistorted radiograph.
3. The mean vertical bone loss is less than 0.2 mm annually after the first year of service.*
4. No persistent pain, discomfort, or infection is attributable to the implant.
5. The implant design does not preclude placement of a crown
or prosthesis with an appearance that is satisfactory to the patient and dentist.
*According to these criteria, a success rate of 85% at the end of a 5-year observation period and 80% at the end of a 10-year period are the minimum
levels for success. May not be applicable to all implants.
486 VOLUME 87 NUMBER 5
proven important to achieving or maintaining osseointegration. 25,26,28 Mombelli et al31 reported no significant difference in the modified plaque index scores of successful implants and failed implants. Some researchers, however, consider the mucosal response to be correlated with marginal bone loss and loss of osseointegration.29,30
Cigarette smoking has been associated with compromised healing and increased implant failures.3,15,32,33 Jensen et al15 found that the implant failure rate in the grafted maxillary sinuses of smokers (12.7%) was more than twice that in non-smokers (4.8%). A retrospective clinical investigation was conducted to determine the effects of implant type, timing of implant placement, pretreatment bone height, oral hygiene status, and patient history of cigarette smoking on the survival of implants placed in grafted maxillary sinuses.
CLINICAL REPORT
A total of 72 patients had implants placed in grafted maxillary sinuses and completed the prosthodontic phase of treatment at Loma Linda University School of Dentistry, Center for Prosthodontics and Implant Dentistry, between 1990 and 1996. Sixty patients returned for follow-up and constituted the population of this report (Table I). The subject population comprised 27 male and 33 female patients between the ages of 41 and 84 years (mean 64.6 years). A total of 228 implants (189 HA-coated [124 threaded and 65 non-threaded] and 39 titanium threaded implants) were placed in 84 grafted maxillary sinuses supporting 69 prostheses (55 fixed partial dentures, 8 fixed complete dentures, 4 overdentures, and 2 single crowns).
Implant survival rates were calculated after implant success was assessed with the criteria proposed by Smith and Zarb,26 where applicable (Table II). Implant prostheses were not removed for individual implant mobility tests unless significant bone loss, peri-implant radiolucency, persistent pain, discomfort, and/or infections were evident.
At the time of data collection, the prostheses had been in function for 0 to 60 months (mean post-prosthetic time of 41.6 months). Thirty-three implants were placed in a combination of autogenous graft (from the iliac or anterior mandibular symphysis) and allograft (demineralized bone) in 11 maxillary sinuses, whereas 195 implants were placed in a combination of xenograft (anorganic bone from bovine sources) and allograft in 73 maxillary sinuses using the lateral wall infracturing technique.10 One hundred fifty-two implants were placed simultaneously with the bone grafting procedure; 76 implants were placed subsequent to maxillary sinus grafting.
Pretreatment bone heights, which represented the presurgical amount of bone present between the floor of the maxillary sinus and the alveolar ridge crest, were measured from the pretreatment panoramic radiographs and reduced to 80% of the original value to compensate for radiograph distortion. Each radiograph was measured (to the nearest 0.5 mm) twice at a 2-week interval, and the mean value was recorded. The recorded values were categorized into low (≤4 mm) and high (>4 mm) bone heights. One examiner made all measurements. The reproducibility of his measurements was determined with the intra-correlation coefficient.
Oral hygiene was evaluated according to the modified plaque index as described by Mombelli et al:31 0 = no detection of plaque, 1 = plaque recognized only by running a probe across the surface of the prostheses supragingivally, 2 = plaque could be seen with unaided vision, 3 = abundance of soft matter. One examiner evaluated the plaque index with the University of North Carolina color probe (Hu-Friedy, Chicago, Ill.) at 4 sites at which the implant attached to the prosthesis: mesiobuccal, mesiolingual, distobuccal, and distolingual. The mean plaque index was calculated by averaging the scores at each site. Oral
MAY 2002 487
hygiene was categorized as good (mean plaque index ≤1), fair (>1 but ≤2), or poor (>2).
Each patient’s smoking history was recorded. Subjects who had never smoked and those who had stopped smoking at least 1 year before implant treatment were classified as non-smokers. Subjects who had smoked cigarettes at least one year before treatment and those who smoked throughout the observation period were classified as smokers. A total of 158 implants were placed in 58 maxillary sinuses in 44 non-smokers, whereas 70 implants were placed in 26 maxillary sinuses in 16 smokers.
Implant survival rates were calculated as the total number of successful implants divided by the total number of implants in the study. Overall implant survival rates were reported as well as individual survival rates according to implant type, simultaneous/delayed implant placement, pretreatment bone height, oral hygiene, and history of cigarette smoking (Table III).
Of the 228 implants placed in grafted maxillary sinuses, 205 (89.9%) remained in function after a mean follow-up period of 41.6 months. Twenty-three failed implants were observed in 8 patients: 4 patients experienced single-implant failures, and the other 4 accounted for the remaining 19 implant failures (Table IV). Two of 39 Ti threaded implants (94.9%), 5 of 124 HA-coated threaded implants (96.0%), and 16 of 65 HA-coated non-threaded implants (75.4%) failed during the observation period.
Implant failure rates according to prosthesis type
488 VOLUME 87 NUMBER 5
were 7.1% (11 of 156 implants) for fixed partial dentures, 12.8% (6 of 47 implants) for fixed complete dentures, 26.1% (6 of 23 implants) for overdentures, and 0% (0 of 2 implants) for implant single crowns. Failure rates according to type of graft material were 11.4% (23 of 202 implants) when a combination of allograft and xenograft were
used and 0% (0 of 26 implants) when a combination of autogenous and allograft were used. Failure rates according to simultaneous or delayed placement were 7.2% (11 of 152 implants) for implants placed simultaneously with sinus grafting and 15.8% (12 of 76 implants) for implants placed subsequent to sinus grafting.
Only 20 of 228 pairs of pretreatment bone height measurements (8.8%) were different, with the largest difference being 1 mm. An intra-correlation coefficient of 99.78% demonstrated significantly high correlation between the 2 measurements (P<.001). Failure rates according to pretreatment bone height were 11.9% (10 of 84 implants) in the low group and 9.1% (13 of 144 implants) in the high group. Failure rates according to oral hygiene status were 1.4% (2 of 143 implants) in patients with good hygiene, 13.8% (9 of 65 implants) in patients with fair hygiene, and 60.0% (12 of 20 implants) in patients with poor hygiene. Failure rates according to smoking status were 17.1% (12 of 70 implants) in the smoker group and 7.0% (11 of 158 implants) in the non-smoker group.
DISCUSSION
The overall survival rate observed in this clinical investigation (89.9%) is comparable to that reported in previous studies (83.0% to 97.0%) for implants placed in grafted maxillary sinuses.9,11,12,15,18 In the present evaluation, a notably higher implant survival rate was recorded for threaded implants (titanium 94.9%; HAcoated 96.0%) than for non-threaded implants (HA-coated 75.4%). This result is in agreement with Brunski,16 who reported that screw-shaped implants provided the strongest retention immediately after implant placement.
The survival rates of implants placed simultaneous with and subsequent to grafting were similar (92.8% and 84.2%, respectively). This is in agreement with the results of other studies.10-12,15 The survival rates observed in relation to pretreatment bone height (88.1% in ≤4 mm bone vs. 90.9% in >4 mm bone) are comparable to those reported by Tidwell et al,11 who found no significant difference in the success rates of implants placed in <5 mm bone (91%) and >5 mm bone (97%). Mombelli et al31 reported no significant difference in the modified plaque index scores associated with successful implants (1.0 ± 0.7) and failed implants (1.3 ± 1.3). Conversely, in the present clinical investigation, 1.4% implant failure was reported for patients with good oral hygiene, 13.9% for patients with fair oral hygiene, and 60.0% for patients with poor oral hygiene. The 2 failed implants in patients with good oral hygiene were classified as such because of implant fracture and unrestorable implant position rather than loss of osseointegration. The results of this clinical report indicate the importance of maintaining good oral hygiene around implants placed in grafted maxillary sinuses.
Of implants placed in smokers and non-smokers, 17.1% and 7.0%, respectively, were classified as failures. These values correspond to the results reported by Jensen et al,15 who found that the implant failure rate in the grafted maxillary sinuses of smokers (12.7%) was more than twice that in non-smokers (4.8%). Based on these results, it can be concluded that cigarette smoking is detrimental to the success of osseointegrated implants placed in grafted maxillary sinuses. Although a controlled prospective study with a larger patient pool may provide more meaningful and powerful information, such a study would be time consuming and expensive. The retrospective nature of this report should be taken into consideration when its results are interpreted. The clinical evaluation was conducted in a teaching institute where treatments were performed by either faculty or graduate students under supervision. Disparity in the experience and expertise of surgeons and restorative dentists may have affected the outcome. Moreover, the 5 variables examined were determined on an individual basis and were not controlled, resulting in significant discrepancies in the sample size for each individual variable. The fact that the 23 failed implants were observed in only 8 patients (19 in 4 patients) suggests that one variable may have confounded the evaluation of another variable. For these reasons, it was virtually impossible to analyze the data in terms of inferential statistics.
Nevertheless, the results from this type of report may provide a basis for the design of a controlled study on a similar subject.
SUMMARY
After a mean post-prosthetic follow-up time of 41.6 months (range 0 to 60 months), 205 of 228 implants placed in grafted maxillary sinuses remained successfully integrated, corresponding to an implant survival rate of 89.9%. Within the population examined, higher failure rates were associated with non-threaded implants, poor oral hygiene, and a patient history of smoking.
MAY 2002 489
REFERENCES
1. Engquist B, Bergendal T, Kallus T, Linden U. A retrospective multicenter evaluation of osseointegrated implants supporting overdentures. Int J Oral Maxillofac Implants 1988;3:129-34.
THE JOURNAL OF PROSTHETIC DENTISTRY KAN ET AL
2. Jaffin RA, Berman CL. The excessive loss of Branemark fixtures in type IV bone: a 5-year analysis. J Periodontol 1991;62:2-4.
3. Bain CA, Moy PK. The association between the failure of dental implants and cigarette smoking. Int J Oral Maxillofac Implants 1993;8:609-15.
4. Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogeneous marrow and bone. J Oral Surg 1980;38:613-6.
5. Tatum H Jr. Maxillary and sinus implant reconstructions. Dent Clin North Am 1986;30:207-29.
6. Jensen OT, Greer RO. Immediate placement of osseointegrated implants into the maxillary sinus augmented with mineralized cancellous allograft and Gore-Tex: second-stage surgical and histological findings. In Laney, WR, Tolman DE, editors. Tissue integration in oral, orthopedic, and maxillofacial reconstruction. Chicago: Quintessence; 1992. p. 321-33.
7. Moy PK, Lundgren S, Holmes RE. Maxillary sinus augmentation: histomorphometric analysis of graft materials for maxillary sinus floor augmentation. J Oral Maxillofac Surg 1993;51:857-62.
8. Boyne PJ, Marx RE, Nevins M, Triplett G, Lazaro E, Lilly LC, Alder M, Nummikoski P. A feasibility study evaluating rhBMP-2/absorbable collagen sponge for maxillary sinus floor augmentation. Int J Periodontics Restorative Dent 1997;17:11-25.
9. Fugazzotto PA, Vlassis J. Long-term success of sinus augmentation using various surgical approaches and grafting materials. Int J Oral Maxillofac Implants 1998;13:52-8.
10. Kent JN, Block MS. Simultaneous maxillary sinus floor bone grafting and placement of hydroxylapatite-coated implants. J Oral Maxillofac Surg 1989;47:238-42.
11. Tidwell JK, Blijdorp PA, Stoelinga PJ, Brouns JB, Hinderks F. Composite grafting of the maxillary sinus for placement of endosteal implants. A preliminary report of 48 patients. Int J Oral Maxillofac Surg 1992;21:204-9.
12. Blomqvist JE, Alberius P, Isaksson S. Retrospective analysis of one-stage maxillary sinus augmentation with endosseous implants. Int J Oral Maxillofac Implants 1996;11:512-21.
13. Wheeler SL, Holmes RE, Calhoun CJ. Six-year clinical and histologic study of sinus-lift grafts. Int J Oral Maxillofac Implants 1996;11:26-34.
14. Hanisch O, Lozada JL, Holmes RE, Cahoun CJ, Kan JY, Spiekermann H. Maxillary sinus augmentation prior to placement of endosseous implants: A histomorphometric analysis. Int J Oral Maxillofac Implants 1999;14:329-36.
15. Jensen OT, Shulaman LB, Block MS, Iacono VJ. Report of the Sinus Consensus Conference of 1996. Int J Oral Maxillofac Implants 1998;13(Suppl):11-45.
16. Brunski JB. Biomechanical factors affecting the bone-dental implant interface. Clin Mater 1992;10:153-201.
17. Buser DA, Schroeder A, Sutter F, Lang NP. The new concept of ITI hollow-cylinder and hollow-screw implants: Part 2. Clinical aspects, indications, and early clinical results. Int J Oral Maxillofac Implants 1988;3:173-81.
18. Wong M, Eulenberger J, Schenk R, Hunziker E. Effect of surface topology on the osseointegration of implant materials in trabecular bone. J Biomed Mater Res 1995;29:1567-75.
19. Lundgren S, Moy P, Johansson C, Nilsson H. Augmentation of the maxillary sinus floor with particulated mandible: a histologic and histomorphometric study. Int J Oral Maxillofac Implants 1996;11:760-6.
20. Raghoebar GM, Brouwer TJ, Reintsema H, Van Oort RP. Augmentation of the maxillary sinus floor with autogenous bone for the placement of endosseous implants: a preliminary report. J Oral Maxillofac Surg 1993;51:1198-203; discussion 1203-5.
21. Hurzeler MB, Kirsch A, Ackermann KL, Quinones CR. Reconstruction of the severely resorbed maxilla with dental implants in the augmented maxillary sinus: a 5-year clinical investigation. Int J Oral Maxillofac Implants 1996;11:466-75.
22. Wennerberg A, Ektessabi A, Albrektsson T, Johansson C, Andersson B. A 1-year follow-up of implants of differing surface roughness placed in rabbit bone. Int J Oral Maxillofac Implants 1997;12:486-94.
23. Misch CE. Maxillary sinus augmentation for endosseous implants: organized alternative treatment plans. Int J Oral Implantol 1987;4:49-58.
24. van Steenberghe D, Klinge B, Linden U, Quirynen M, Herrmann I, Garpland C. Periodontal indices around natural teeth and titanium abutments. a longitudinal multicenter study. J Periodontol 1993;64:538-41.
25. Lekholm U, Adell R, Lindhe J, Branemark PI, Eriksson B, Rockler B, Lindvall AM, Yoneyama T. Marginal tissue reactions at osseointegrated titanium fixtures. (II) A cross-sectional retrospective study. Int J Oral Maxillofac Surg 1986;15:53-61.
26. Smith DE, Zarb GA. Criteria for success of osseointegrated endosseous implants. J Prosthet Dent 1989;62:567-72.
27. Adell R, Lekholm U, Rockler B, Branemark PI, Lindhe J, Eriksson B, Sbordone L. Marginal tissue reactions at osseointegrated titanium fixtures.
(I) A 3-year longitudinal prospective study. Int J Oral Maxillofac Surg 1986;15:39-52.
28. Apse P, Zarb GA, Schmitt A, Lewis DW. The longitudinal effectiveness of osseointegrated dental implants. The Toronto Study: peri-implant mucosal response. Int J Periodontics Restorative Dent 1991;11:94-111.
29. Teixeira ER, Sato Y, Akagawa Y, Kimoto T. Correlation between mucosal inflammation and marginal bone loss around hydroxyapatite-coated implants: a 3-year cross-sectional study. Int J Oral Maxillofac Implants 1997;12:74-81.
30. Block MS, Kent JN. Long-term follow-up on hydroxyapatite-coated cylindrical dental implants: a comparison between developmental and recent periods. J Oral Maxillofac Surg 1994;52:937-43; discussion 944.
31. Mombelli A, van Oosten MA, Schurch E Jr, Lang NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 1987;2:145-51.
32. Kan JY, Rungcharassaeng K, Lozada JL, Goodacre CJ. Effects of smoking on implant success in grafted maxillary sinuses. J Prosthet Dent 1999;82:307-11.
33. Small SA, Zinner ID, Panno FV, Shapiro HJ, Stein JI. Augmenting the maxillary sinus for implants: report of 27 patients. Int J Oral Maxillofac Implants 1993;8:523-8.
Reprint requests to:
DR JOSEPH Y. K. KAN
DEPARTMENT OF RESTORATIVE DENTISTRY
LOMA LINDA UNIVERSITY SCHOOL OF DENTISTRY
LOMA LINDA, CA 92350
FAX: (909)558-4803
E-MAIL: jkan@sd.llu.edu
Copyright © 2002 by The Editorial Council of The Journal of Prosthetic
Dentistry.
0022-3913/2002/$35.00 + 0. 10/1/124202