articol-alsheri-2017
ORAL IMPLANTOLOGY
A COMPREHENSIVE REVIEW OF SYSTEMIC FACTORS ASSOCIATED WITH PERI-
Review Article
IMPLANT DISEASES
Mohammed Alshehri1a*
¹Dental Department, King Khalid University Hospital, King Saud University, Riyadh, Saudi Arabia
BDS, AEGD, SSC-ARD, SF-DI, Consultant in Cosmetic Restorative and Implant Dentistry
a
Received: February 01, 2017
Revised: February 23, 2017
Accepted: March 06, 2017
Published: March 07, 2017
Academic Editor: Constantinus Politis, MD, DDS, MM, MHA, PhD, Professor and Chairperson, University of Leuven, Leuven, Belgium
Cite this article:
Alshehri M. A comprehensive review of systemic factors associated with periimplant diseases. Stoma Edu J. 2017;4(1):37-43.
ABSTRACT DOI: 10.25241/stomaeduj.2017.4(1).art.3
Background: A variety of systemic factors have been associated with peri-implant diseases.
Objective: The aim of the present comprehensive review was to assess current literature regarding
the systemic factors associated with the etiology of peri-implant diseases.
Results: Both normal and premalignant oral mucosa cells (NOK and POE9i) displayed uptake
of PLGAChiNPs in a time and concentration-dependent manner, both in 2D and 3D models. A
higher and more rapid uptake of PLGAChi NPs by precancerous cell line POE9i was observed
when compared to NOKs. Interestingly, DPCs did not display internalized PLGAChi NPs, even at the
highest concentration of 200 g/mL.
Data source: Databases were searched till January 2017 using different combinations of the following
key words: “acquired immune deficiency syndrome”; “cancer”; “diabetes mellitus”; “genetic”; “peri-
implant diseases”; “peri-implantitis”, “renal”; and “risk-factors”.
Study selection: Clinical studies assessing the systemic factors associated with the etiology of peri-
implantitis were included. Letters to the Editor, case-reports, case-series, in-vitro studies, studies on
animal models and commentaries were excluded.
Data extraction: The pattern of the present comprehensive review was customized to primarily
summarize the pertinent information.
Data synthesis: Poorly-controlled diabetes mellitus (DM) is a significant risk factor for peri-implant
diseases; however, under optimal glycemic control dental implants can osseointegrate in patients
with DM. Osteoporosis and rheumatoid arthritis have been associated with peri-implant diseases;
however, implant surface modifications and optimal oral hygiene maintenance are essential
parameters that can facilitate osseointegration in these patients. Although irradiation is a significant
risk-factor for peri-implant diseases; studies have shown that osseointegration and survival of
implants is possible in cancer patients. There is a weak evidence that HIV infection is no more a
contradiction for implant therapy. Although systemic diseases are significant risk-factors for dental
implant failure, proper management of the systemic disorder and optimal oral hygiene may support
osseointegration and survival of dental implants in medically-compromised patients.
Keywords: acquired immune deficiency syndrome, cancer, diabetes mellitus, genetic, peri-implant
diseases.
1. Introduction implants.4, 5 According to a consensus report from
Although studies1-3 have reported implant the 6th European Workshop on Periodontology,
success and survival rates of up to 100%; a peri-implantitis is defined as the presence of
number of systemic factors have been reported inflammation of the peri-implant mucosa and
to jeopardize the success and survival of dental concurrent loss of supporting alveolar bone.6
*Corresponding author:
Dr Mohammed Alshehri, BDS, AEGD, SSC-ARD, SF-DI, Dental Department, King Khalid, University Hospital, King Saud University, Riyadh, Saudi Arabia.
Tel/Fax: +96.655.380.333 / +966.114.672.428, e-mail: dr_mzs@hotmail.com
Stomatology Edu Journal 37
A COMPREHENSIVE REVIEW OF SYSTEMIC FACTORS ASSOCIATED WITH PERI-IMPLANT DISEASES
Mombelli et al.7 described peri-implantitis as a site- also been associated with the etiology of peri-
Review Article specific inflammatory condition, which displays implantitis cannot be disregarded (Fig. 1).17-21
clinical and radiographic features that are similar Considering the length of the article, the author
to those in patients with chronic periodontitis. dedicated the present article to comprehensively
Data regarding the prevalence of peri-implantitis review the systemic risk-factors associated with
is inconsistent. In the study by Koldsland et the etiology of peri-implantitis. The aim of the
al.,8 the prevalence of peri-implantitis ranged present comprehensive review was to provide
between 11.3% and 47.1%; whereas Mombelli an overview of current literature regarding the
et al.9 reported peri-implantitis in 20% of their systemic conditions associated with the etiology
study population during 5 to 10 years of follow- of peri-implantitis.
up. In the study by Zitzmann and Berglundh,6
the frequency of peri-implantitis varied between 2. Materials and methods
28% and at least 56% of the participants and 2.1. Focused question
12% and 43% of individual implants. Peri-implant The addressed focused question was “Which
diseases are categorized into two types namely, systemic conditions are associated with the
peri-implant mucositis and peri-implantitis. Peri- etiology of peri-implant diseases?”
implant mucositis is characterized by inflammation 2.2. Literature search strategy
of soft tissues around the implant without any PubMed/Medline, Scopus, EMBASE, ISI Web of
signs of peri-implant alveolar bone loss.6 Patients knowledge and Google-Scholar databases were
with peri-implant mucositis exhibit bleeding on searched from till January 2017 using the following
probing (BOP), peri-implant probing depth ≥ key words: “arthritis”, “cancer”, “diabetes mellitus”;
4mm and/or suppuration.10,11 “acquired immune deficiency syndrome”;
A variety of factors, local as well as systemic “renal disorders”; “osteoporosis”, “peri-implant/
factors have been associated with the etiology of periimplant” and “genetics”.
peri-implantitis.12-16 It is well known that poor oral Clinical studies assessing the local risk-factors
hygiene, tobacco smoking, poor bone quality and associated with the etiology of peri-implant
quantity, jaw location and bruxism are among diseases were included.
the most common local factors associated with 2.3. Eligibility criteria
the etiology of peri-implantitis. Nevertheless, Results from only clinical studies were included.
the contribution of systemic factors such as Letters to the Editor, historic reviews, case-reports,
immunosuppression (as observed in patients case-series, in-vitro studies, studies on animal
with acquired immune deficiency syndrome, models and commentaries were excluded. The
osteoporosis, poorly-controlled diabetes mellitus pattern of the present comprehensive review was
and cancer) and use of medications (such as customized to primarily summarize the pertinent
bisphosphonates and corticosteroids) that have information.
Figure 1. Systemic factors associated with peri-implant diseases.
38 Stoma Edu J. 2017;4(1):37-43. http://www.stomaeduj.com
A COMPREHENSIVE REVIEW OF SYSTEMIC FACTORS ASSOCIATED WITH PERI-IMPLANT DISEASES
3. Results two main categories of BPs are the “non-nitrogen”
Review Article
3.1. Diabetes mellitus and “nitrogen-containing” BPs.40 Non–nitrogen-
Diabetes mellitus (or diabetes) is a common containing BPs are metabolized rapidly, whereas
metabolic disorder characterized by hypergly-cemia nitrogen-containing BPs are much more potent and
due to impaired insulin secretion, insufficient insulin are not metabolized.41 These drugs act by inhibiting
action, or both.22 The main types of diabetes include osteoclastic activity and inducing their apoptosis.18
type 1 diabetes and type 2 diabetes. Type 1 diabetes BPs may be administered by either oral or
is associated with pancreatic beta (β)-cell destruction intravenous routes. Oral BPs are used in the treatment
and accounts for 5-10% of the subjects with diabetes. of diseases such as osteoporosis and Pagets’
Type 2 diabetes is associated with a relative, rather disease; while intravenous BPs are administered to
than an absolute insulin deficiency and accounts patients with breast cancer, multiple myeloma, bone
for 90-95% of all individuals with diabetes.23 metastasis and malignant hypercalcemia. The chief
Individuals with poorly-controlled diabetes are more complication observed in patients under either oral
susceptible to develop complications after implant or intravenous BP therapy is osteonecrosis of the jaw
therapy compared to individuals with well-controlled (ONJ).42 It has been suggested that all patients under
diabetes.24 bisphosphonate therapy who are expected to receive
Chronic hyperglycemia has been related with tissue dental implants should be informed of the possible
damage, since endothelial cells take up glucose risks of development of ONJ and consequent
passively in an insulin-independent manner.25,26 implant loss beforehand; and an informed-consent
Hyperglycemia is also associated with an altered must be obtained prior to installation of dental
host resistance, for example, defective migration implants in these individuals.14,15
of polymorphonuclear leukocytes, impaired Although, the risk of developing ONJ in patients
phagocytosis and an exaggerated inflammatory using BPs is estimated to be minimal (approximately
response to microbial products.27 0.09%), there still exists a controversy over the
The treatment of diabetes focuses on the attainment placement of dental implants in patients treated
of an optimal glycemic control in order to impede with BPs.43 Results from case-reports44-47 have
complications. shown that dental implants can osseointegrate
Individuals with diabetes are more susceptible to and remain functionally stable in patients under
periodontal disease, which is also recognized as the BP therapy. Similar results have been reported
sixth complication of diabetes.28-32 in retrospective studies.48,49 Results by Bell and
The underlying pathophysiology that increases Bell50 showed comparable implant survival rates
the risk of periodontal bone loss in subjects with between patients using BPs and controls, that is,
diabetes is poorly understood; however it has been 95% and 96.5% respectively. Brooks et al.47 placed
associated with the formation and accumulation of 10 implants in a patient on bisphosphonate therapy
glucose-mediated advanced glycation end-products out of which, 9 implants osseointegrated successfully
(AGEs). giving a success rate of 90%. Likewise, results from
AGEs accumulate in the plasma and tissues (including a case-report by Wang et al.44 also showed implant
the periodontium) during the process of normal healing to be uneventful with no alterations in the
aging, but to an accelerated degree in subjects healing process of dental implants in a patient
with diabetes.33 AGEs contribute to periodontal using BPs. Fugazzotto et al.51 showed that a history
destruction by activating receptors called “Receptor of bisphosphonate therapy was not associated
for AGEs (RAGE)” located on the periodontium with the occurrence of ONJ following installation of
and by reducing the production of matrix proteins, immediately-loaded dental implants.
such as collagen and osteocalcin by gingival and In their systematic review, Javed and Almas18
periodontal fibroblasts.34-38 reported that the incidence of implant failure in
It has been suggested that the pathogenesis of patients taking BPs is minimal.
diabetes and its complications are associated with The authors also concluded that placement of dental
an increased RAGE expression.29,39 implants in patients taking BPs can have a positive
Other cell types with RAGE expression include outcome.18
glomerular epithelial cells (podocytes), endothelial 3.3. Osteoporosis and rheumatoid arthritis
cells, vascular smooth muscle cells, inflammatory Osteoporosis is a metabolic disease of bone
mononuclear phagocytes and lymphocytes.39 characterized by low bone mineral density
Therefore, an impaired glycemic status may (BMD) and reduced bone mass due to impaired
negatively affect the outcome of implant therapy. In bone metabolism and imbalanced osteoblastic
a systematic review, Javed and Romanos19 reported and osteoclastic activities.52,53 In osteoporotic
that under optimal glycemia control, dental implants bone, osteoblasts demonstrate impaired pro-
can osseointegrate and remain functionally stable liferative, synthetic and reactive ability to cellular
over long durations in patients with diabetes. mediators.52,54,55
3.2. Bisphosphonates Underlying causes of osteoporosis include pre- and
Bisphosphonates (BPs), (such as alendronate, postmenopausal estrogen deficiency, excessive
risendronate, ibandronate, and clodronate) are glucocorticoid intake, eating disorders such as
important group of drugs used for the treatment anorexia nervosa and celiac disease.56,57 Although
of metabolic and oncologic pathologies involving the bone quality and strength are compromised in
the skeletal system. The mode of action of BPs osteoporotic patients; osteoporosis is not considered
depends on the drugs’ chemical structure. The a contraindication for implant the-rapy.58,59 In a recent
Stomatology Edu Journal 39
A COMPREHENSIVE REVIEW OF SYSTEMIC FACTORS ASSOCIATED WITH PERI-IMPLANT DISEASES
systematic review, Javed et al.60 assessed the effect dental implantation ranged from 6 to 15 months.
Review Article of osteogenic coatings on the osseointegration of The overall implant failure rate of 9.53% and
implants under induced osteoporotic conditions. osseointegration success rates ranged between
Nearly 80% studies reported that osteogenic 62.5% and 100%.67 In another review, Javed et al.20
coatings around implant surfaces enhance bone assessed the implant survival rate after oral cancer
formation, bone-to-implant contact (BIC) and bone therapy. In total, 21 studies were included in this
volume (BV) under osteoporosis-like conditions. review out of which, 16 studies reported that dental
This could possibly be accredited to the increase implants can osseointegrate and remain functionally
in surface roughness of the implant caused by stable in patients having undergone radiotherapy
osteogenic coatings, which facilitate the attachment following oral cancer surgery.20 The authors
of osteoprogenitor cells to the implant surface. concluded that dental implants can osseointegrate
Holahan et al.59 conducted a retrospective study and remain functionally stable in patients having
to evaluate whether a diagnosis of osteoporosis undergone oral cancer treatment.20
affected the survival rate of osseointegrated dental 3.5. Human immunodeficiency virus infection
implants. In this study59, a total of 3,224 implants Human immunodeficiency virus (HIV) infection is
placed in 746 female patients aged at least 50 years characterized by progressive immune system failure
old at the time of implant placement were assessed. that gives rise to the development of opportunistic
The results showed that patients with a diagnosis of infections and neoplasms. The virus invades CD4+
osteoporosis or osteopenia were not significantly T lymphocytes, macrophages and dendritic cells,
more likely to develop implant failure compared to and the CD4+ T cell counts gradually decrease as a
those without such a diagnosis.59 result of direct cytopathic action or cytotoxic CD8+T
Krennmair et al.61 evaluated the implant treat-ment lymphocyte-mediated attack. In a recent systematic
outcomes for patients suffering from autoimmune review, Ata-Ali et al.68 attempted to answer the
rheumatoid arthritis (RA) with or without concomitant following focused question “does HIV infection have
connective tissue diseases (CTD). In this study,61 34 an impact upon dental implant osseointegration?”
female patients (25 iso-lated RA; nine RA+CTD) were The combinations of search terms resulted in a
included. At the mean duration of follow-up of nearly list of 132 titles. Consequently, 101 studies were
46 month, all implants presented a survival rate of excluded on the basis of the evaluation of the title
100%. In isolated RA patients, acceptable marginal and abstract, thereby leaving 9 articles for eligibility
bone loss (MBL) (mean: 2.1 mm; SD: 0.5 mm), pocket assessment. Amongst the studies included in this
depth (mean: 2.8 mm; SD:3.2 mm) and healthy soft- systematic review, a total of 173 dental implants were
tissue conditions (plaque/bleeding/gingiva index placed in 80 patients (135 implants in 56 HIV-positive
Grade 0 in 80%) were observed.61 Results from a case- individuals and 38 implants in 24 HIV-negative
series report,62 showed a high implant survival rate patients -control groups). A single loss of dental
during follow-up with a cumulative 3-year implant implant osseointegration was recorded in an HIV-
success rate of 96.1%. In this study, RA patients positive patient.68 In the study by Stevenson et al.69,
demonstrated acceptable MBL (mean: 2.1 +/- 0.5 40 dental implants were placed in 20 HIV-infected
mm) and satisfactory soft tissue conditions; whereas patients. No implant osseointegration failures were
CTD patients showed increased MBL (mean: 3.1 +/- recorded after 6 months of follow-up. Similarly, in
0.7 mm). another study of 39 dental implants placed in 24
The study62 concluded that a high implant and HIV-infected patients, no implant osseointegration
prosthodontic success rate can be anticipated in failures were recorded after 12 months of follow-
patients suffering from RA; however, the authors up.70 Should dental implants placed in HIV positive
emphasized that optimal oral hygiene assists in patients sustain bone levels in the long-term (5 years
ensuring stable long-term survival of dental implants or longer) requires further investigations.
in patients with RA.62 3.6. Genetic factors
3.4. Irradiation Jacobi-Gresser et al.71 assessed diagnostic markers
Osteoradionecrosis is usually observed several to predict titanium implant failure.
years following radiotherapy and is associated with The study reported that tumor necrosis factor-alpha
local trauma within the hypovascular–hypocellular (TNF-α) and interleukin 1-beta (IL-1β) release on
hypoxic tissues (that occurs as a result of radiation- titanium stimulation were significantly higher among
induced endarteritris).63 In this regard, the interval patients with implant failure.
between the end of cancer therapy and placement The results showed that IL-1β/TNF-α release and
of dental implants may contribute to the success number of risk genotypes were significantly
or failure of osseointegration. Studies64-66 have associated with implant failure.71
investigated the required time interval between Vaz et al.72 examined IL-1 gene clusters in 155 patients
radiotherapy and implant installation that may with 100 successful implants and 55 unsuccessful
influence osseointegration; however the results implants.
remain debatable. In a systematic review, Zen Filho The authors concluded that successful implants
et al.67 assessed the safety of dental implants placed were associated with a negative genetic test and
in irradiated bone and to discuss their viability that unsuccessful implants were associated with a
when placed post-radiotherapy. Eight publications positive genetic test.72
were assessed in this systematic review67 and the Casado and colleagues reported that the IL-6
results showed a total of 331 patients received 1237 genotype was 1.53 times more likely to convey peri-
implants. The time interval between irradiation and implant disease if the individuals had the GC
40 Stoma Edu J. 2017;4(1):37-43. http://www.stomaeduj.com
A COMPREHENSIVE REVIEW OF SYSTEMIC FACTORS ASSOCIATED WITH PERI-IMPLANT DISEASES
genotype and allele G. may support osseointegration and survival of dental
Review Article
implants in medically-compromised patients.
4. Conclusion
Although systemic diseases such as poorly controlled Conflict of interest and financial disclosure
DM, RA and osteoporosis are significant risk-factors The author reports no conflict of interest and there
for dental implant failure, proper management of was no external source of funding for the present
the systemic disorder and optimal oral hygiene study.
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Mohammed ALSHEHRI
BDS, AEGD, SSC-ARD, SF-DI
Dental Department, King Khalid
University Hospital King Saud
University, Riyadh, Saudi Arabia
CV
Dr Alshehri graduated from the College of Dentistry, King Saud University in 2001. Academically, he has
acquired a Certificate in Advanced Education in General Dentistry at the University of Southern California,
School of Dentistry. Thereafter, Dr Alshehri joined the SBARD Program wherein he obtained the Saudi Specialty
Certificate in Advanced Restorative Dentistry. Subsequently, he was able to obtain a Certificate for Saudi
Fellowship in Dental Implant and is currently a Fellow of International Team for Implantology (ITI). Professionally,
Dr Alshehri has conducted multiple research projects, has obtained a number of patents and has made local
and international presentations. Currently, Dr Alshehri is a Consultant in Cosmetic, restorative and implant
dentistry at College of Medicine and University Hospitals and board member of the Saudi Dental Society.
Questions
Osteoradionecrosis is usually observed several years following radiotherapy; and is associated
with local trauma within the hypovascular–hypocellular hypoxic tissues.
q a. The first statement is true but the second statement is false;
q b. The first statement is false but the second statement is true;
q c. Both statements are true;
q d. Both statements are false.
Osteoporosis is a metabolic disease of bone characterized by:
q a. low bone mineral density;
q b. reduced bone mass due to impaired bone metabolism;
q c. imbalanced osteoblastic activity;
q d. all of the above.
The mode of action of bisphosphonates depends on the drugs’:
q a. Physical structure;
q b. Chemical structure;
q c. Half-life;
q d. Side-effects.
All of the following are local risk-factors of peri-implant diseases EXCEPT:
q a. Implant diameter;
q b. Tobacco smoking;
q c. Poor bone quality;
q d. Quantity of bone.
Stomatology Edu Journal 43