Osteoporosis and Dental Implant Outcomes

Ira Lamster DDS, MMSc, Editor-in-Chief, Fiona Collins BDS, MBA, MA, FPFA

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Osteoporosis and Dental Implant Outcomes

Osteoporosis is a skeletal condition in which mineral is lost from bones, resulting in an increased risk of fracture. Bone resorption and bone deposition occur physiologically throughout life.

Osteoporosis results from resorption outpacing deposition, and changes in structural integrity make fracture more likely. Patients with osteoporosis have a bone mass density (BMD) at least 2.5 standard deviations below the benchmark, which is the BMD of a healthy 30-year-old of the same gender.1Pitts NB, Zero DT, Marsh PD, Ekstrand K, Weintraub JA, Ramos-Gomez F, Tagami J, Twetman S, Tsakos G, Ismail A. Dental caries. Nat Rev Dis Primers 2017;25(3):17030.,2JD. The caries balance: the basis for caries management by risk assessment. Oral Health Prev Dent 2004;2(Suppl 1):259-64. This is represented as a T-score of ≤-2.5 versus the benchmark. Osteopenia is an intermediate condition between normal bone density and osteoporosis, and is defined as a T-score between ≤-1 to >-2.5.2Featherstone JD. The caries balance: the basis for caries management by risk assessment. Oral Health Prev Dent 2004;2(Suppl 1):259-64. As a result of its potential impact in the maxilla and mandible, the effect of osteoporosis on the placement and long-term survival of dental implants has been examined.3Shuler CF. Inherited risks for susceptibility to dental caries. J Dent Educ 2001;65(10):1038-45. Given the low BMD seen with osteoporosis, there has been concern that the rate of bone-to-implant contact, bone support and implant survival may be impaired in patients with osteoporosis.4Opal S, Garg S, Jain J, Walia I. Genetic factors affecting dental caries risk. Aust Dent J 2015;60:2-11.,5Bretz WA, Corby PM, Melo MR, Coelho MQ, Costa SM, Robinson M, Schork NJ, Drewnowski A, Hart TC. Heritability estimates for dental caries and sucrose sweetness preference. Arch Oral Biol 2006;51(12):1156-60.,6Nibali L, Di Iorio A, Tu YK, Vieira A. Host genetics role in the pathogenesis of periodontal disease and caries. J Clin Periodontol 2017;44:S18:52-78.,7Lips A, Antunes LS, Pintor AVB, dos Santos DAB, Bachinski R, Küchler EC, Alves GG. Salivary protein polymorphisms and risk of dental caries: a systematic review. Braz Oral Res 2017;31:e41.

Implant survival rates and marginal bone loss

A recent systematic review and meta-analysis of 15 studies included almost 9,000 patients with close to 30,000 implants placed in individuals with and without osteoporosis.8Wang X, Shaffer JR, Weyant RJ, Cuenco KT, DeSensi RS, Crout R, McNeil DW, Marazita ML. Genes and their effects on dental caries may differ between primary and permanent dentitions. Caries Res 2010;44:277-84. The data indicated no statistically significant differences in implant survival at the individual implant level (relative risk was 1.39; p=0.11) or at the patient level (relative risk 0.98; p=0.94). While 0.18 mm greater marginal bone loss was found for implants placed in persons with osteoporosis (p=0.005), it was unclear if this had any clinical relevance as implant survival did not differ.8Wang X, Shaffer JR, Weyant RJ, Cuenco KT, DeSensi RS, Crout R, McNeil DW, Marazita ML. Genes and their effects on dental caries may differ between primary and permanent dentitions. Caries Res 2010;44:277-84. An earlier review examined the influence of several factors on the risk for failure of dental implants.6 Four of 51 studies evaluated the influence of osteoporosis on implant survival in 3,070 implants. A direct association was found for risk of implant failure in patients with osteoporosis, but did not reach statistically significance (RR=1.09; p=0.14). However, the researchers noted that the severity of osteoporosis was not addressed in the studies and that all were retrospective, ranging from 9 months to 10 years in length.6Nibali L, Di Iorio A, Tu YK, Vieira A. Host genetics role in the pathogenesis of periodontal disease and caries. J Clin Periodontol 2017;44:S18:52-78.
Further, a non-randomized multicenter study of implant outcomes in older women (59 to 83 years-of-age; mean age 67 years) with and without osteoporosis/osteopenia has recently been published.4Opal S, Garg S, Jain J, Walia I. Genetic factors affecting dental caries risk. Aust Dent J 2015;60:2-11. At one year after functional loading, implant survival and marginal bone loss were evaluated for 46 of 48 patients with screw-retained or bar overdenture implant-supported restorations. Implants placed in women with osteoporosis/osteopenia demonstrated comparable survival rates to implants placed in women without osteoporosis/osteopenia (on the implant level, 98.4% vs. 100% survival rate; p=0.43); on the person level, 94.7% vs. 100%; p=0.417). In addition, while marginal bone loss in patients with osteoporosis/osteopenia occurred mainly after functional loading and in patients without osteoporosis/osteopenia before functional loading, there were no statistically significant differences in absolute marginal bone loss at one year.4Opal S, Garg S, Jain J, Walia I. Genetic factors affecting dental caries risk. Aust Dent J 2015;60:2-11.
Implants placed in women with and without osteoporosis/osteopenia have demonstrated comparable survival rates.
A recent retrospective cross-sectional study examined peri-implant marginal bone loss (MBL) in women with and without osteoporosis (mean age 64 years).3Shuler CF. Inherited risks for susceptibility to dental caries. J Dent Educ 2001;65(10):1038-45. At one year, proximal bone loss was more pronounced adjacent to implants placed in women with osteoporosis. Mean mesial and distal MBL were -1.1 mm ±-1.3, and -1.2 mm ±1.3, respectively, vs. -0.6 ±1.2 mm and -0.5 mm ±1.3, respectively, in women with (n=18) and without (n=30) osteoporosis. (Figure 1) This difference was significant after adjusting for confounders, including smoking and treatment with bisphosphonates (BP). Study limitations included the short evaluation period of one year, and some but not all patients were treated with vitamin D or BP. Additionally, 7 patients were diagnosed with osteoporosis prior to, 4 at the time of, and 7 subsequent to implant placement, Osteoporosis was not considered a contraindication for implant placement in women with osteoporosis.3Shuler CF. Inherited risks for susceptibility to dental caries. J Dent Educ 2001;65(10):1038-45.
In a retrospective study of more than 4,000 patients with over 13,000 implants placed between 2004 and 2012, 81 patients had a history of osteoporosis (1.9%).7Lips A, Antunes LS, Pintor AVB, dos Santos DAB, Bachinski R, Küchler EC, Alves GG. Salivary protein polymorphisms and risk of dental caries: a systematic review. Braz Oral Res 2017;31:e41. The up-to-8-year survival rate was 94.4% for patients with osteoporosis, with no statistically significant difference in survival rate compared with healthy patients without osteoporosis (p=0.661). However, failure rates for patients with osteoporosis were higher in the maxilla than the mandible, and it was suggested that anatomical differences in bone microarchitecture might play a role.7Lips A, Antunes LS, Pintor AVB, dos Santos DAB, Bachinski R, Küchler EC, Alves GG. Salivary protein polymorphisms and risk of dental caries: a systematic review. Braz Oral Res 2017;31:e41. In another study with a mean follow-up of more than 5 years, 79 elderly patients with lowered BMD received implant-supported mandibular overdentures.9Corby PM, Bretz WA, Hart TC, Schork NJ, Wessel J, Lyons-Weiler J, Paster BJ. Heritability of oral microbial species in caries-active and caries-free twins. Twin Res Hum Genet 2007;10(6):821-8. The implant survival rate was 98.7%, and on examination of 63 available patients no association was found for BMD and the amount of MBL (p=0.466). It was concluded that osteoporosis was not a contraindication for implant therapy.9Corby PM, Bretz WA, Hart TC, Schork NJ, Wessel J, Lyons-Weiler J, Paster BJ. Heritability of oral microbial species in caries-active and caries-free twins. Twin Res Hum Genet 2007;10(6):821-8.

Figure 1. Mean marginal bone loss in women with and without osteoporosis3Shuler CF. Inherited risks for susceptibility to dental caries. J Dent Educ 2001;65(10):1038-45.


In a retrospective study, the up-to-8-year survival rate was 94.4% for patients with osteoporosis and similar to the rate for healthy patients without osteoporosis.

Other reviews and studies have also failed to find evidence for osteoporosis as an absolute or relative contraindication for implant placement, including a recent qualitative review in which the implant survival rate was similar for patients with and without osteoporosis.10Papapostolou A, Kroffke B, Tatakis DN, Nagaraja HN, Kumar PS. Contribution of host genotype to the composition of health-associated supragingival and subgingival microbiomes. J Clin Periodontol 2011;38:517-24.,11Gomez A, Espinoza JL, Harkins DM, Leong P, Saffery R, Bockmann M, Torralba M, Kuelbs C, Kodukula R, Inman J, Hughes T, Craig JM, Highlander SK, Jones MB, Dupont CL, Nelson KE. Host genetic control of the oral microbiome in health and disease. Cell Host Microbe 2017;22:269-78 e263.,12Shaffer JR, Wang X, McNeil DW, Weyant RJ, Crout R, Marazita ML. Genetic susceptibility to dental caries differs between the sexes: a family-based study. Caries Res 2015;49:133-40.,13Stahringer SS, Clemente JC, Corley RP, Hewitt J, Knights D, Walters WA, Knight R, Krauter KS. Nurture trumps nature in a longitudinal survey of salivary bacterial communities in twins from early adolescence to early adulthood. Genome Res 2012;22:2146-52. One study has also assessed peri-implantitis, finding no significant differences in the percentage of implants with peri-implantitis, evaluated for up to 10 years after insertion, for patients with and without osteoporosis.14Momeni SS, Whiddon J, Cheon K, Ghazal T, Moser SA, Childers NK. Genetic diversity and evidence for transmission of streptococcus mutans by DiversiLab rep-PCR. J Microbiol Methods 2016;128:108-17.

Implant stability

In one study, it was observed that MBL was significantly greater in the maxilla than the mandible for patients with osteoporosis, leading to the conclusion that achieving primary stability may differ for the two jaws.3Shuler CF. Inherited risks for susceptibility to dental caries. J Dent Educ 2001;65(10):1038-45. In a separate study, implant stability was assessed using resonance frequency analysis for 49 patients with and without osteoporosis.15Paglia L, Scaglioni S, Torchia V, De Cosmi V, Moretti M, Marzo G, Giuca MR. Familial and dietary risk factors in early childhood caries. Eur J Paediatr Dent 2016;17:93-9. While statistically significant differences were found for implant stability when comparing patients with osteoporosis to patients with a physiologically healthy BMD, implant osseointegration was achieved for all patient groups. Primary stability measured as the implant stability quotient (ISQ) was 63.3 ± 10.3, 65.3 ± 7.5 and 66.7 ± 8.7 ISQ, respectively, for patients with osteoporosis, osteopenia and without either condition (Figure 2). Following osseointegration, implant stability at the time of abutment placement measured 66.4 ± 9.5, 70.7 ± 7.8, and 72.2 ± 7.2 ISQ, respectively.15Paglia L, Scaglioni S, Torchia V, De Cosmi V, Moretti M, Marzo G, Giuca MR. Familial and dietary risk factors in early childhood caries. Eur J Paediatr Dent 2016;17:93-9.

Figure 2. Primary implant stability and stability at abutment placement (ISQ)

 

Implant surface morphology

Significantly less MBL has been observed to occur around rough-surface implants compared to machined (smooth surface) implants in patients with osteoporosis.3Shuler CF. Inherited risks for susceptibility to dental caries. J Dent Educ 2001;65(10):1038-45. Further, in a recent systematic review examining the impact of surface coatings on dental implants placed in osteoporotic bone in 6 laboratory studies, bone volume and bone-in-contact (BIC) were found in 5 of the 6 studies to be significantly greater for implants with osteoinductive and osteoproliferative coatings compared to non-coated implants.16Kong Y-Y, Zheng J-M, Zhang W-J, Jiang Q-Z, Yang X-C, Yu M, Zeng SuJ. The relationship between vitamin D receptor gene polymorphism and deciduous tooth decay in Chinese children. BMC Oral Health 2017;17:111. Laboratory studies also indicate that microrough-surface implants result in greater tissue maturation at 3 days and osseointegration at 14 days than is observed for machined surfaces under conditions of reduced BMD.17American Dental Association. Symposium on Early Childhood Caries in American Indian and Alaska Native Children, 2010.

Anti-resorptive therapy in patients with osteoporosis

The risk of implant failure and osteonecrosis of the jaw (ONJ) in patients with osteoporosis receiving anti-resorptive therapy, typically bisphosphonates (BP), is a further consideration.18Vieira AR, Marazita ML, Goldstein-McHenry T. Genome-wide scan finds suggestive caries loci. J Dent Res 2008;87(5):435-9. A prevalence of ≤0.1% was estimated for BP-induced ONJ for this patient population in one review.19Vieira AR, Modesto A, Marazita ML. Caries: review of human genetics research. Caries Res 2014;48:491-506. A more recent position paper reported an overall prevalence close to 0% (range 0.00038% to 0.1%) for patients receiving oral BP for <4 years, and up to 0.21% for longer-term use of oral BP.20Acton RT, Dasanayake AP, Harrison RA, Li Y, Roseman JM, Go RCP, Wiener H, Caufield PW. Association of MHC genes with levels of caries-inducing organisms and caries severity in African-American women. Human Immunol 1999;60:984-9. In another review, in most studies implant failure was not observed in patients with osteoporosis receiving BP therapy within the study timeframes.18Vieira AR, Marazita ML, Goldstein-McHenry T. Genome-wide scan finds suggestive caries loci. J Dent Res 2008;87(5):435-9.
In a systematic review with meta-analysis of 8 studies with more than 4,500 implants placed, insufficient evidence was found for any impact of BP on implant survival.21Bagherian A, Nematollahi H, Afshari JT, Moheghi N. Comparison of allele frequency for hla-dr and hla-dq between patients with ecc and caries-free children. J Indian Soc Pedod Prev Dent 2008;26:18-21. However, informed consent about the risk of long-term implant failure and low risk of BP-ONJ is advised. It is also suggested that, in consultation with the patient’s medical provider and depending on the patient’s condition and the risk versus benefit, that consideration be given to stopping BP therapy for 2 months prior to implant placement and until osseous healing has occurred, or changing the dose, or using a different drug.20Acton RT, Dasanayake AP, Harrison RA, Li Y, Roseman JM, Go RCP, Wiener H, Caufield PW. Association of MHC genes with levels of caries-inducing organisms and caries severity in African-American women. Human Immunol 1999;60:984-9.
In a systematic review with meta-analysis of 8 studies with more than 4,500 implants placed, insufficient evidence was found for any impact of BP on implant survival.

Conclusions

Osteoporosis is not a contraindication to implant treatment. As populations age, an increasing number of people will require dental implants to maintain oral function, and may present with or subsequently develop osteoporosis. Patients must be informed of the risks, including increased MBL around implants and implant failure.20Acton RT, Dasanayake AP, Harrison RA, Li Y, Roseman JM, Go RCP, Wiener H, Caufield PW. Association of MHC genes with levels of caries-inducing organisms and caries severity in African-American women. Human Immunol 1999;60:984-9. Patients should also be educated about the need for sound oral hygiene practices and regular dental care for on-going evaluation.19Vieira AR, Modesto A, Marazita ML. Caries: review of human genetics research. Caries Res 2014;48:491-506.,20Acton RT, Dasanayake AP, Harrison RA, Li Y, Roseman JM, Go RCP, Wiener H, Caufield PW. Association of MHC genes with levels of caries-inducing organisms and caries severity in African-American women. Human Immunol 1999;60:984-9. Lastly, there is a need for additional, well-designed, longer-duration and larger sample size studies to assess the impact of severity of osteoporosis on implant survival, as well as the effect of comorbidities such as smoking or diabetes mellitus, and the impact of BP therapy.6Nibali L, Di Iorio A, Tu YK, Vieira A. Host genetics role in the pathogenesis of periodontal disease and caries. J Clin Periodontol 2017;44:S18:52-78.,8Wang X, Shaffer JR, Weyant RJ, Cuenco KT, DeSensi RS, Crout R, McNeil DW, Marazita ML. Genes and their effects on dental caries may differ between primary and permanent dentitions. Caries Res 2010;44:277-84.10Papapostolou A, Kroffke B, Tatakis DN, Nagaraja HN, Kumar PS. Contribution of host genotype to the composition of health-associated supragingival and subgingival microbiomes. J Clin Periodontol 2011;38:517-24.,21Bagherian A, Nematollahi H, Afshari JT, Moheghi N. Comparison of allele frequency for hla-dr and hla-dq between patients with ecc and caries-free children. J Indian Soc Pedod Prev Dent 2008;26:18-21.

References

  • 1.Pitts NB, Zero DT, Marsh PD, Ekstrand K, Weintraub JA, Ramos-Gomez F, Tagami J, Twetman S, Tsakos G, Ismail A. Dental caries. Nat Rev Dis Primers 2017;25(3):17030.
  • 2.JD. The caries balance: the basis for caries management by risk assessment. Oral Health Prev Dent 2004;2(Suppl 1):259-64.
  • 3.Shuler CF. Inherited risks for susceptibility to dental caries. J Dent Educ 2001;65(10):1038-45.
  • 4.Opal S, Garg S, Jain J, Walia I. Genetic factors affecting dental caries risk. Aust Dent J 2015;60:2-11.
  • 5.Bretz WA, Corby PM, Melo MR, Coelho MQ, Costa SM, Robinson M, Schork NJ, Drewnowski A, Hart TC. Heritability estimates for dental caries and sucrose sweetness preference. Arch Oral Biol 2006;51(12):1156-60.
  • 6.Nibali L, Di Iorio A, Tu YK, Vieira A. Host genetics role in the pathogenesis of periodontal disease and caries. J Clin Periodontol 2017;44:S18:52-78.
  • 7.Lips A, Antunes LS, Pintor AVB, dos Santos DAB, Bachinski R, Küchler EC, Alves GG. Salivary protein polymorphisms and risk of dental caries: a systematic review. Braz Oral Res 2017;31:e41.
  • 8.Wang X, Shaffer JR, Weyant RJ, Cuenco KT, DeSensi RS, Crout R, McNeil DW, Marazita ML. Genes and their effects on dental caries may differ between primary and permanent dentitions. Caries Res 2010;44:277-84.
  • 9.Corby PM, Bretz WA, Hart TC, Schork NJ, Wessel J, Lyons-Weiler J, Paster BJ. Heritability of oral microbial species in caries-active and caries-free twins. Twin Res Hum Genet 2007;10(6):821-8.
  • 10.Papapostolou A, Kroffke B, Tatakis DN, Nagaraja HN, Kumar PS. Contribution of host genotype to the composition of health-associated supragingival and subgingival microbiomes. J Clin Periodontol 2011;38:517-24.
  • 11.Gomez A, Espinoza JL, Harkins DM, Leong P, Saffery R, Bockmann M, Torralba M, Kuelbs C, Kodukula R, Inman J, Hughes T, Craig JM, Highlander SK, Jones MB, Dupont CL, Nelson KE. Host genetic control of the oral microbiome in health and disease. Cell Host Microbe 2017;22:269-78 e263.
  • 12.Shaffer JR, Wang X, McNeil DW, Weyant RJ, Crout R, Marazita ML. Genetic susceptibility to dental caries differs between the sexes: a family-based study. Caries Res 2015;49:133-40.
  • 13.Stahringer SS, Clemente JC, Corley RP, Hewitt J, Knights D, Walters WA, Knight R, Krauter KS. Nurture trumps nature in a longitudinal survey of salivary bacterial communities in twins from early adolescence to early adulthood. Genome Res 2012;22:2146-52.
  • 14.Momeni SS, Whiddon J, Cheon K, Ghazal T, Moser SA, Childers NK. Genetic diversity and evidence for transmission of streptococcus mutans by DiversiLab rep-PCR. J Microbiol Methods 2016;128:108-17.
  • 15.Paglia L, Scaglioni S, Torchia V, De Cosmi V, Moretti M, Marzo G, Giuca MR. Familial and dietary risk factors in early childhood caries. Eur J Paediatr Dent 2016;17:93-9.
  • 16.Kong Y-Y, Zheng J-M, Zhang W-J, Jiang Q-Z, Yang X-C, Yu M, Zeng SuJ. The relationship between vitamin D receptor gene polymorphism and deciduous tooth decay in Chinese children. BMC Oral Health 2017;17:111.
  • 17.American Dental Association. Symposium on Early Childhood Caries in American Indian and Alaska Native Children, 2010.
  • 18.Vieira AR, Marazita ML, Goldstein-McHenry T. Genome-wide scan finds suggestive caries loci. J Dent Res 2008;87(5):435-9.
  • 19.Vieira AR, Modesto A, Marazita ML. Caries: review of human genetics research. Caries Res 2014;48:491-506.
  • 20.Acton RT, Dasanayake AP, Harrison RA, Li Y, Roseman JM, Go RCP, Wiener H, Caufield PW. Association of MHC genes with levels of caries-inducing organisms and caries severity in African-American women. Human Immunol 1999;60:984-9.
  • 21.Bagherian A, Nematollahi H, Afshari JT, Moheghi N. Comparison of allele frequency for hla-dr and hla-dq between patients with ecc and caries-free children. J Indian Soc Pedod Prev Dent 2008;26:18-21.