Periodontal disease: associations with diabetes, glycemic control and complications
Oral Diseases (2008) 14, 191–203. doi:10.1111/j.1601-0825.2008.01442.xÓ 2008 The Authors. Journal compilation Ó 2008 Blackwell MunksgaardAll rights reserved
Periodontal disease: associations with diabetes, glycemiccontrol and complications
1School of Dentistry and 2School of Public Health, University of Michigan, Ann Arbor, MI, USA
OBJECTIVE: This report reviews the evidence for ad-
verse effects of diabetes on periodontal health and peri-
Diabetes mellitus and periodontal disease are two
odontal disease on glycemic control and complications of
common chronic diseases that have long been consid-
ered to be biologically linked. Diabetes is an important
DESIGN: MEDLINE search of the English language litera-
chronic disease globally as reﬂected in the World
ture identified primary research reports published on (a)
Health Organization (WHO) declaring the rate of
relationships between diabetes and periodontal diseases
increase in diabetes prevalence is an epidemic. The
since 2000 and (b) effects of periodontal infection on gly-
WHO estimated there were 30 million people who had
cemic control and diabetes complications since 1960.
diabetes worldwide in 1985. This number increased to
RESULTS: Observational studies provided consistent
135 million by 1995, and reached 217 million in 2005.
evidence of greater prevalence, severity, extent, or pro-
By 2030 WHO predicts this number to increase to at
gression of at least one manifestation of periodontal
least 366 million (Smyth and Heron, 2006). This
disease in 13/17 reports reviewed. Treatment and longi-
growth in diabetes prevalence, driven principally by
tudinal observational studies provided evidence to sup-
increasing prevalence of type 2 diabetes, is occurring in
port periodontal infection having an adverse effect on
both developing and developed countries. The two
glycemic control, although not all investigations reported
countries with the largest predicted increases are India
an improvement in glycemic control after periodontal
and China and the US ranked third (Smyth and Heron,
treatment. Additionally, evidence from three observa-
tional studies supported periodontal disease increasing
Susceptible individuals with diabetes and those with
the risk for diabetes complications and no published
chronically poor metabolic control can experience
microvascular and macrovascular complications leading
CONCLUSION: The evidence reviewed supports diabe-
to a signiﬁcant burden for the individual and society.
tes having an adverse effect on periodontal health and
This burden includes direct costs of medical care and
periodontal infection having an adverse effect on glyce-
indirect costs, such as lost productivity, which result
mic control and incidence of diabetes complications.
from diabetes-related morbidity and premature mortal-
Further rigorous study is necessary to establish unequiv-
ity (Harris, 1995; Hogan et al, 2003). Health care
ocally that treating periodontal infections can contribute
spending for people with diabetes is more than double
to glycemic control management and to the reduction of
what spending would be without diabetes, and direct
the burden of diabetes complications.
and indirect expenditures attributable to diabetes in
2002 in the US were conservatively estimated at $132billion, with slightly more spent on chronic complica-
Keywords: periodontal disease; diabetes; epidemiology; peri-
tions attributable to diabetes than on diabetes care itself
(Hogan et al, 2003). The International Diabetes Feder-ation estimated that diabetes accounts for 5–10% of thetotal healthcare budget in many countries (Smyth and
Correspondence: George W Taylor, School of Dentistry and School of
Public Health, University of Michigan, 1011 N. University, Ann
Gingivitis and periodontitis are the most common
Arbor, MI 48109, USA. Tel: 734 764 1737, Fax: 734 936 1597, E-mail:
periodontal diseases. For example, in the US approxi-
mately 50% of the population in all age groups exhibit
There are no ﬁnancial relationships that may pose a conﬂict of
reversible gingival inﬂammation (Albandar and King-
man, 1999). Moderate or severe periodontitis, with
Received 29 June 2007; revised 13 December 2007; accepted 15December 2007
destruction of periodontal attachment tissues is much
less common than gingivitis yet still a common chronic
been proposed to result in pertubation of cellular
disease, aﬀecting approximately 5–15% of any popula-
properties, exaggerated and sustained inﬂammatory
tion (Albandar et al, 1999; Burt, 2005).
response, impaired wound healing, and more severe
Current evidence regarding the biologic link between
diabetes-associated periodontal disease (Lalla et al,
diabetes and periodontal disease supports diabetes and
persisting hyperglycemia leading to an exaggerated
The speciﬁc ways in which diabetes-enhanced inﬂam-
immuno-inﬂammatory response to the periodontal
mation and apoptosis may speciﬁcally impact on peri-
odontal tissues of was recently thoroughly reviewed
2006; Nishimura et al, 2007), resulting in more rapid
(Graves et al, 2006). In their review, Graves and
and severe periodontal tissue destruction. In the meta-
colleagues describe that diabetes has been reported to
bolic dysregulation of diabetes, persisting hyperglycemia
adversely aﬀect bone repair by decreasing expression of
causes non-enzymatic glycation and oxidation of pro-
genes that induce osteoblast diﬀerentiation, and dimin-
teins and lipids, and the subsequent formation of
ishing growth factor and extracellular matrix production
advanced glycation endproducts (AGEs), which accu-
(Bouillon, 1991; Kawaguchi et al, 1994; Lu et al, 2003).
mulate in the plasma and tissues (Brownlee, 1994;
One proposed mechanism for these adverse eﬀects is
Schmidt et al, 1996b; Ramasamy et al, 2005). Hyper-
through the contribution of AGEs to decreased extra-
glycemia and resultant AGE formation are considered
cellular matrix production and inhibition of osteoblast
to be a major causal factor in the pathogenesis of
diﬀerentiation (McCarthy et al, 2001; Cortizo et al,
2003; Santana et al, 2003). AGEs may also delay
1994). In subjects with diabetes who also have peri-
wound-healing by inducing apoptosis of extracellular-
odontitis, AGEs with accompanying markers for
matrix-producing cells. This enhanced apoptosis would
increased oxidant stress have been demonstrated in
reduce the number of osteoblastic and ﬁbroblastic cells
human gingiva (Schmidt et al, 1996a). Cell surface
available for the repair of resorbed alveolar bone
binding sites or receptors for AGE (RAGE) have been
(Graves et al, 2006). In addition to promoting apopto-
identiﬁed on the cell surfaces of several cell types
sis, AGEs could aﬀect oral tissue healing by reducing
exhibiting a heightened inﬂammatory response and
expression of collagen and promoting inﬂammation.
involved with the pathogenesis of complications of
The mechanisms suggested for AGE-enhanced apopto-
diabetes. These cell types include mononuclear phago-
sis include the direct activation of caspase activity, and
cytes, endothelial cells, ﬁbroblasts, smooth muscle cells,
indirect pathways that increase oxidative stress or the
lymphocytes, podocytes, and neurons (Brett et al, 1993;
expression of pro-apoptotic genes that regulate apopto-
Ramasamy et al, 2005). The receptor for AGEs, RAGE,
is the principal signal transducer for the AGE ligand(Schmidt et al, 2000).
The underlying postulate associated with these ﬁnd-
ings is that enhanced oxidant stress in the gingivaltissues could contribute to more frequent and more
Evidence establishing the link between diabetes mellitus
severe periodontal tissue destruction in individuals with
and adverse eﬀects on periodontal health have been
diabetes. For example, it has been hypothesized that the
extensively reviewed (Taylor, 2001; Mealey et al, 2006).
AGE-RAGE interaction induces an oxidant stress that
In a narrative review of the English language literature
may contribute to chronic monocytic upregulation,
published between 1960 and 2000 Taylor (2001)
activation of NF-jB, and subsequent expression of
reported that 44 of 48 observational studies provided
mRNA and secretion of proinﬂammatory cytokines
supportive evidence of diabetes adversely aﬀecting
(such as TNF-a, IL-1b, and IL-6) by monocytic
periodontal health provided (37 of the 41 cross-sectional
phagocytes involved in periodontal tissue inﬂammation
and seven of the seven cohort studies).
and destruction (Baeuerle, 1991; Schreck et al, 1991;
The review conducted for this current report extends
Moughal et al, 1992; Collins, 1993; Schmidt et al, 1994,
that 2001 review to include reports published into 2007.
1996a; Takahashi et al, 1994; Yan et al, 1994). These
The search used MEDLINE as well as reviewed
mediators are recognized as eﬀectors in periodontal
reference lists of relevant papers obtained from the
tissue inﬂammation and destruction (Salvi et al, 1998).
search to identify primary research reports on investi-
Blockade of RAGE has been shown to diminish
gations of relationships between diabetes/diabetes con-
Porphyromonas gingivalis-triggered alveolar bone loss
trol and periodontal diseases/periodontal treatment.
in the periodontium and limit the enhanced inﬂamma-
While the literature review is extensive in conducting
tory response in peripheral wounds, accelerating wound
the MEDLINE search, it is not exhaustive in that no
closure and facilitating angiogenesis (Lalla et al, 2000;
other databases were searched. This review does not
Goova et al, 2001). Additionally, AGE interaction with
provide a formal assessment of the quality of the
endothelial cell RAGE has been shown to enhance
reports. The reports identiﬁed are displayed in table-
endothelial cell vascular hyperpermeability and expres-
form and the corresponding description is organized
sion of vascular cell adhesion molecule-1, an adherence
according to the following groupings of studies: (1) The
molecule capable of attracting mononuclear cells to the
eﬀects of having diabetes on periodontal diseases in
vascular wall (Schmidt et al, 1995; Wautier et al, 1996;
studies that include a non-diabetes comparison group
Lalla et al, 1998b). Hence, AGE-RAGE interaction has
(Table 1) and (2) Eﬀect of the degree of glycemic
Periodontal disease and diabetesGW Taylor and WS Borgnakke
control, usually measured by level of glycosylated
increasing attention with greater numbers of publica-
hemoglobin, on periodontal status in studies that
tions in consecutive decades, ranging from six in the
included assessment of degree of glycemic control while
1960s, eight in the 1970s, and 12 in the 1980s to 20 in the
evaluating periodontal status in participants with dia-
1990s. This review identiﬁed 17 reports published in
the current decade starting in the year 2000. Table 1
The reports included in Table 1 were restricted to
presents a summary of the evidence on the relationship
studies which compared periodontal health in subjects
between diabetes and periodontal disease. Studies were
with and without diabetes. This subject has attracted
broadly classiﬁed and ordered by type of diabetes and
Table 1 Effects of diabetes on periodontal diseases in studies including a non-diabetes control group; ordered by diabetes type and subject age
Duration of diabetesDiabetes severity based onpresence of complications
aDM type = diabetes type: 1 = type 1 diabetes mellitus; 2 = type 2 diabetes mellitus; 1,2 = both subjects with type 1 and type 2 diabetes mellitusincluded; GDM = gestational diabetes mellitus; 9 = diabetes type not speciﬁed and not clearly ascertainable from other information in the report.
bAges: subjects’ ages presented as minimum – maximum reported for those with a. diabetes (DM) and b. controls (Control) unless otherwisespeciﬁed.
cMeasure of periodontal disease status: Measures used include Ging = gingivitis or gingival bleeding, Ppd = probing pocket depth, Lpa = loss ofperiodontal attachment, XRBL = radiographic bone loss, JPS = juvenile periodontal score, MGI = modiﬁed gingival index, PI = Russell’sPeriodontal Index, PDR = periodontal disease rate (proportion of teeth aﬀected by periodontal disease). The number following the measurecorresponds to greater disease in those with diabetes (1) or no diﬀerence between those with diabetes and controls (0). The letters following thenumber correspond to the parameter(s) assessed in the study: e = extent, i = incidence, p = prevalence, s = severity, r = progression.
Table 2 Effect of degree of glycemic control on periodontal status, ordered by level of evidence, diabetes type, and subject age
aHierarchy of evidence based on classiﬁcation scheme used (U.S. Preventive Services Task Force, 1996) where: I = evidence obtained from at leastone properly randomized controlled trial; II-1 = evidence obtained from well-designed controlled trial without randomization; II-2 = evidenceobtained from well-designed cohort or case-control analytic studies, preferably from more than one center or research group; II-3 = evidenceobtained from multiple time series with or without the intervention. Dramatic results in uncontrolled experiments (such as the results of theintroduction of penicillin treatment in the 1940s) could also be regarded as this type of evidence; III = opinions of respected authorities, based onclinical experience; descriptive studies and case reports; or reports of expert committees.
bDiabetes type: 1 = type 1 diabetes mellitus; 2 = type 2 diabetes mellitus; 1,2 = both subjects with type 1 and type 2 diabetes mellitus included;GDM = gestational diabetes mellitus; 9 = diabetes type not speciﬁed and not clearly ascertainable from other information in the report;*= diabetes type not speciﬁed but ascertained by reviewers from other information in the report or from other sources, such as directcommunication with the authors.
cEﬀect: 1 = subjects with poorer glycemic control had poorer health than the comparison group(s); 0 = no diﬀerence in the periodontal healthstatus between subjects with poorer glycemic control and comparison group(s).
dDiabetes types are 1 and 2 for all but one subject who had drug-induced diabetes mellitus.
age of subjects (Table 1). In contrast to seven reports of
study included children only (Lalla et al, 2007), and all
prospective studies published prior to 2000, all of the
other studies included adult subjects, although one also
studies identiﬁed for this review are cross-sectional
included children or adolescents (Arrieta-Blanco et al,
and thus limited in their ability to provide evidence for
2003). Two of these three studies reported greater
causal inferences. There was one study of type 1 diabetes
prevalence, extent, or severity of periodontal disease
and it reported more extensive radiographic bone loss
for at least one measure or index of periodontal disease
in participants with type 1 diabetes (Tervonen et al,
(Arrieta-Blanco et al, 2003; Lalla et al, 2007). One
report did not ﬁnd signiﬁcant diﬀerences in periodontal
Regarding the relationship between type 2 diabetes
disease between subjects with and without diabetes
and periodontitis the review identiﬁed 10 reports. One
report comprised 15–45+ year olds (Endean et al, 2004),
Two studies report on analyses on National Health
and nine (Sandberg et al, 2000; Orbak et al, 2002; Tsai
and Nutrition Examination Survey III data from over
et al, 2002; Zielinski et al, 2002; Lu and Yang, 2004;
4000 women with a history of gestational diabetes
Campus et al, 2005; Chuang et al, 2005; Borges-Ya´n˜ez
(GDM) in the US. One report included ages 15–44
et al, 2006; Mattout et al, 2006) included only adults.
(Xiong et al, 2006) the other ages 20–59 (Novak et al,
Seven of these 10 studies reported signiﬁcantly poorer
2006). Both reports concluded there is a strong rela-
periodontal health in subjects with type 2 diabetes,
tionship between GDM and periodontal disease. Xiong
whereas no signiﬁcant diﬀerence was discerned in a study
et al (2006) found periodontitis in 45% of pregnant
of mostly older Taiwanese dialysis patients with and
women with GDM vs 13% in the group without
without Ôinsulin-dependent (type II) diabetes’ (Chuang
diabetes, with an adjusted odds ratio of 9.11. In non-
et al, 2005) as well as in a study of U. S. university clinic
pregnant women, 40% of women with type 1 or 2
patients 60+ years of age with good medical and dental
diabetes, 25% of those with a history of GDM, and
care comparing well-controlled (mean HbA1c = 7.3%
14% of women without diabetes had periodontal
with 70% having HbA1c > 7.5%) subjects with diabe-
disease. The odds ratio for those with type 1 and 2
tes to subjects without diabetes (Zielinski et al, 2002);
diabetes was 2.76 (Xiong et al, 2006). Novak et al (2006)
whereas in a study of Mexicans 60+ years of age there
found the prevalence of periodontal disease to be higher
in women with a history of GDM and concluded that
(P = 0.09) of periodontitis in the group with diabetes
women with at history of GDM may be at greater risk
(61.5%) than in the group without diabetes (49.5%)
for developing more severe periodontal disease. A
smaller Greek study of 34–36 weeks pregnant women
Several reports consist of analyses in which subjects
also concluded gingival inﬂammation was more pre-
with type 1 and type 2 diabetes were not distinguished.
valent in the women with GDM (Mittas et al, 2006), but
All of the studies in this subset were cross-sectional. One
also found more plaque in that group.
Periodontal disease and diabetesGW Taylor and WS Borgnakke
As with other complications of diabetes, current
periodontal infection adversely aﬀecting glycemic con-
evidence also supports poorer glycemic control contrib-
trol in diabetes and contributing to increased risk for
uting to poorer periodontal health. Primary research
the pathogenesis of diabetes complications. Because of
reports in the literature published since 2000 investigat-
the high vascularity of the inﬂamed periodontium, this
ing relationships between glycemic control level and
inﬂamed tissue may serve as an endocrine-like source
periodontal disease have included studies with subjects
with type 1 diabetes exclusively (one study), type 2
(Oﬀenbacher et al, 1996; Grossi and Genco, 1998).
diabetes exclusively (seven studies), or a combination of
Because of the predominance of Gram-negative anaer-
individuals with either type 1 or type 2 diabetes (three
obic bacteria in periodontal infection, the ulcerated
studies) (Table 2). Only seven of the 12 reports pub-
pocket epithelium is thought to constitute a chronic
lished regard the association between degree of glycemic
source of systemic challenge from bacteria, bacterial
control and periodontal disease speciﬁcally in type 2
products and locally produced inﬂammatory media-
diabetes (Sandberg et al, 2000; Tsai et al, 2002; Lu and
tors. TNF-a, IL6, and IL1, all mediators important in
Yang, 2004; Campus et al, 2005; Chuang et al, 2005;
periodontal inﬂammation, have been shown to have
Jansson et al, 2006; Peck et al, 2006). Five of the latter
important eﬀects on glucose and lipid metabolism,
found poorer glycemic control to be a signiﬁcant factor
particularly following an acute infectious challenge or
associated with poorer periodontal health, the associa-
trauma (Feingold et al, 1989; Ling et al, 1995; Grossi
tion was borderline signiﬁcant in one study of dialysis
and Genco, 1998). TNF-a has been reported to
patients (Chuang et al, 2005) and no diﬀerence was
interfere with lipid metabolism and to be an insulin
found in the remaining study (Sandberg et al, 2000).
antagonist (Grunfeld et al, 1990; Feingold and Grun-
Among the studies providing information on diﬀerences
feld, 1992). IL6 and IL1 have also been reported to
in periodontal health classiﬁed by glycemic control
antagonize insulin action (Ling et al, 1995; Michie,
status, most have been cross-sectional, with eight of 12
publications reporting more prevalent or more severe
More direct, empirical evidence regarding the eﬀects of
periodontal disease in those with poorer glycemic
periodontal infection on glycemic control of diabetes
control (Tervonen et al, 2000; Tsai et al, 2002; Guzman
comes from treatment studies using non-surgical peri-
et al, 2003; Lu and Yang, 2004; Negishi et al, 2004;
odontal therapy and observational studies (Table 3). The
Campus et al, 2005; Jansson et al, 2006; Peck et al,
treatment studies are a heterogeneous set of reports that
2006) and four reporting no diﬀerences (Sandberg et al,
include randomized clinical trials (RCTs) and non-
RCTs. The RCTs used control groups that were either
Murtomaa, 2003; Chuang et al, 2005). There was one
non-treated controls (Aldridge et al, 1995; Kiran et al,
follow-up study identiﬁed (evidence level II-2) that was
2005), positive controls (Grossi et al, 1997; Rodrigues
published since 2000 (Karikoski and Murtomaa, 2003).
et al, 2003; Skaleric et al, 2004), or controls advised to
The preponderance of studies included in this review
continue with their usual source of dental care (Jones
of reports published since 2000 on the adverse eﬀects of
et al, 2007). Of the seven RCTs, four reported a beneﬁcial
diabetes on periodontal health are cross-sectional and
eﬀect for periodontal therapy (Grossi et al, 1997; Rodri-
describe ﬁndings of convenience samples, principally
gues et al, 2003; Skaleric et al, 2004; Kiran et al, 2005).
from outpatients in hospitals and clinics. While limita-
An important source of variation in the RCTs is the
tions on causal inference must be considered, these
use of adjunctive antibiotics with the non-surgical
reports continue to support previous consistent evidence
periodontal therapy. Among the RCTs, four included
of greater prevalence, severity or extent of at least one
adjunctive antibiotics used systemically (Grossi et al,
manifestation of periodontal disease in the large major-
1997; Rodrigues et al, 2003; Jones et al, 2007) or
ity of studies. The reports reviewed also provide
delivered locally (Skaleric et al, 2004). Three of these
additional evidence to support a Ôdose-response’ rela-
four RCTs using antibiotics showed beneﬁcial eﬀects on
tionship, i.e., as glycemic control worsens, the adverse
glycemic control (Grossi et al, 1997; Rodrigues et al,
eﬀects of diabetes on periodontal health become greater.
2003; Skaleric et al, 2004). However, it is important to
Further, focused study of the relationship between
note the signiﬁcant improvement for one study was in
gestational diabetes and periodontal health is emerging
the positive control group that did not receive the
systemic antibiotic (Rodrigues et al, 2003) and one of
Finally, the ﬁndings and conclusions from this review
the four RCTs reporting a beneﬁcial eﬀect did not use
are consistent with two published meta-analyses that
antibiotics (Kiran et al, 2005). Hence, to date there is no
have provided quantitative summaries of the adverse
clear-cut evidence to support a requirement for the use
eﬀects of diabetes on periodontal health (Papapanou,
of antibiotics in combination with non-surgical peri-
odontal treatment in order to observe an improvementin glycemic control associated with periodontal therapy.
Among the set of thirteen periodontal treatment
Periodontal disease: its effects on glycemic
studies that were not RCTs, eight reported a beneﬁcial
control and complications of diabetes mellitus
eﬀect on glycemic control (Williams and Mahan,
In addition to the substantial evidence demonstrating
1960; Wolf, 1977; Miller et al, 1992; Seppala et al,
diabetes as a risk factor for poor periodontal health,
1993; Seppala and Ainamo, 1994; Iwamoto et al, 2001;
there is a growing body of evidence supporting
Faria-Almeida et al, 2006; Schara et al, 2006) and ﬁve
Periodontal disease and diabetesGW Taylor and WS Borgnakke
Periodontal disease and diabetesGW Taylor and WS Borgnakke
did not (Smith et al, 1996; Westfelt et al, 1996; Christ-
likely to have prevalent proteinuria, and cardiovascu-
gau et al, 1998; Promsudthi et al, 2005; Talbert et al,
lar complications including stroke, transient ischemic
2006). Only two of these studies had control or
attacks, angina, myocardial infarction, and intermit-
comparison groups (Stewart et al, 2001; Promsudthi
tent claudication than controls at their follow-up
et al, 2005). Like the RCTs there was marked variation
in the use of adjunctive antibiotics, with three of the ﬁve
Two recent reports from the on-going longitudinal
studies that used systemic antibiotics reporting a ben-
study of diabetes and its complications in the Gila River
eﬁcial eﬀect on glycemic control (Williams and Mahan,
Indian Community in Arizona, USA, conducted by the
1960; Miller et al, 1992; Iwamoto et al, 2001).
National Institute of Diabetes and Digestive and Kidney
As shown in Table 3, there is marked heterogeneity in
Diseases, address nephropathy and cardiovascular dis-
the studies’ designs, conduct, length of follow-up, types
ease. Saremi et al (2005) studied a cohort of 628
of participants, and periodontal treatment protocols.
individuals for a median follow-up time of 11 years.
The details of the variation in this body of literature
Individuals with severe periodontal disease had 3.2 times
have been extensively described in several detailed
greater risk for cardio-renal mortality (i.e., ischemic
reviews (Grossi and Genco, 1998; Taylor, 1999; Janket
heart disease and diabetic nephropathy combined) than
those with no, mild, or moderate periodontal disease.
Additional evidence to support the eﬀect of severe
This estimate of signiﬁcantly greater risk persisted while
periodontitis on increased risk for poorer glycemic
controlling for several major risk factors of cardio-renal
control comes from two longitudinal observational
mortality including: age, sex, diabetes duration, HbA1c,
studies. A longitudinal epidemiological study of the
body mass index (BMI), hypertension, blood glucose,
Pima Indians in Arizona, USA (Taylor et al, 1996)
cholesterol, electrocardiographic abnormalities, macro-
found subjects with type 2 diabetes in good to moderate
control and with severe periodontitis at baseline were
In the second report Shultis et al (2007) investigated
approximately six times more likely to have poor
the eﬀect of periodontitis on risk for development overt
glycemic control at approximately 2-years follow-up
nephropathy (macroalbuminuria) and end-stage renal
than those without severe periodontitis at baseline. In
disease (ESRD) in a group of 529 Gila River Indian
another observational study of 25 adults with type 2
Community adults with type 2 diabetes. Their propor-
diabetes, aged 58–77 years, Collin et al (1998) also
tional hazards models analyses, adjusted for age, sex,
reported an association between advanced periodontal
diabetes duration, body mass index, and smoking,
disease and impaired metabolic control.
indicated periodontitis and edentulism were signiﬁcantly
It is well recognized that poor glycemic control is a
associated with the risk of overt nephropathy and
major determinant for the development of the chronic
ESRD. The incidence of macroalbuminura was 2.0, 2.1,
complications of diabetes. Results from the landmark
and 2.6 times greater in individuals with moderate or
Diabetes Control and Complications Trial (type 1
severe periodontitis or in those who were edentulous,
diabetes) and the UK Prospective Diabetes Study
respectively, than those with none/mild periodontitis.
(type 2 diabetes) demonstrated that attaining and
The incidence of ESRD was also 2.3, 3.5, and 4.9 times
maintaining good glycemic control could reduce the
greater for individuals with moderate or severe perio-
risk for and slow the progression of microvascular
dontitis or for those who were edentulous, respectively,
complications in patients with type 1 and type 2
than those with none/mild periodontitis.
diabetes (Anonymous, 1993, 1998a,b) (Diabetes Con-
The clinical and epidemiological evidence reviewed
trol and Complications Trial Research Group, 1993).
provides support for the concept that periodontal
Additionally, the UKPDS observed a 16% reduction
infection contributes to poorer glycemic control and
(P = 0.052) in the risk of combined fatal or nonfatal
the risk for diabetes complications in people with
myocardial infarction and sudden death. Further
diabetes mellitus. However, further rigorous, controlled
epidemiological analysis from the UKPDS showed a
trials in diverse populations are warranted to ﬁrmly
continuous association between the risk of cardio-
establish that treating periodontal infections can be
vascular complications and glycemia; every percentage
inﬂuential in contributing to glycemic control manage-
point decrease in HbAlc (e.g., 9–8%), was associated
ment and possibly to the reduction of the burden of
with 25% reduction in diabetes-related deaths, 7%
reduction in all-cause mortality, and 18% reduction incombined fatal and nonfatal myocardial infarction
There is emerging evidence from observational
The evidence reviewed in this report supports previous
studies regarding the association between periodontal
conclusions that diabetes is associated with increased
occurrence and progression of periodontitis and peri-
Thorstensson et al (1996) studied 39 case-control pairs
odontal infection is associated with poorer glycemic
of individuals with type 1 and type 2 diabetes for
control in people with diabetes. There is also evidence
6 years median follow-up time in Jo¨nko¨ping, Sweden.
emerging that gestational diabetes may adversely aﬀect
In each pair the cases had severe alveolar bone loss
periodontal health. Additionally, evidence is emerging
and controls had gingivitis or minor alveolar bone
to suggest that periodontal disease is associated with
loss. They found that cases were signiﬁcantly more
increased risk for diabetes complications. While treating
Periodontal disease and diabetesGW Taylor and WS Borgnakke
periodontal infection in people with diabetes is clearly
Borges-Ya´n˜ez SA, Irigoyen-Camacho ME, Maupome G
an important component in maintaining oral health, it
(2006). Risk factors and prevalence of periodontitis in
may also have an important role in establishing and
community-dwelling elders in Mexico. J Clin Periodontol 33:
maintaining glycemic control and possibly in delaying
the onset or progression of diabetes complications.
Bouillon R (1991). Diabetic bone disease. Calcif Tissue Int 49:
Further rigorous, systematic study in diverse popula-
Brett J, Schmidt AM, Yan SD et al (1993). Survey of the
tions is warranted to support existing evidence that
distribution of a newly characterized receptor for advanced
treating periodontal infections can be inﬂuential in
glycation end products in tissues. Am J Pathol 143: 1699–
contributing to glycemic control management and
possibly to the reduction of the burden of complications
Brownlee M (1994). Lilly Lecture 1993. Glycation and diabetic
complications. Diabetes 43: 836–841.
Burt BA (2005). Position paper: epidemiology of periodontal
diseases. J Periodontol 76: 1406–1419.
Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G (2005).
Diabetes and periodontal disease: a case-control study.
Drs. Taylor and Borgnakke both searched the literature
for reports for possible inclusion in this manuscript.
Christgau M, Palitzsch KD, Schmalz G, Kreiner U, Frenzel S
Both authors reviewed reports, conferred on which
(1998). Healing response to non-surgical periodontal
articles to include, and completed article assessment
therapy in patients with diabetes mellitus: clinical, micro-
forms, designed by Dr. Taylor, to summarize the
biological, and immunologic results. J Clin Periodontol 25:
content of relevance to this literature review for each
included report. Dr. Taylor designed the format for the
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