Dental caries, diabetes mellitus, metabolic control and diabetes duration: A systematic review and meta‐analysis

Abstract

Objective:
To analyze articles aimed at evaluating the association between diabetes, metabolic control, diabetes duration, and dental caries.

Overview:
A systematic search in PubMed, Cochrane Library, Embase, and Web of Science was conducted to retrieve papers in English, Portuguese, and Spanish, up to April 2019. The research strategy was constructed considering the "PECO" strategy. Only quantitative observational studies were analyzed. The risk of bias was assessed using the Newcastle-Ottawa Quality Assessment Scale. The meta-analyses were performed based on random-effects models using the statistical platform R. A total of 69 articles was included in the systematic review and 40 in the meta-analysis. Type 1 diabetics have a significantly higher DMFT compared to controls. No significant differences were found between type 2 diabetics and controls and between well-controlled and poorly controlled diabetics. Concerning diabetes duration, all authors failed to find differences between groups.

Conclusion:
Although there is still a need for longitudinal studies, the meta-analysis proved that type 1 diabetics have a high dental caries risk.

Clinical significance:
It is necessary to be aware of all risk factors for dental caries that may be associated with these patients, making it possible to include them into an individualized prevention program.

Full text

REVIEW ARTICLE
Dental caries, diabetes mellitus, metabolic control and diabetes
duration: A systematic review and meta-analysis
Ana Sofia Coelho
1,2,3,4,5
| Inês Flores Amaro
1
| Francisco Caramelo
2,3,4,5,6
|
Anabela Paula
1,2,3,4,5
| Carlos Miguel Marto
1,2,3,4,5,7
|
Manuel Marques Ferreira
2,3,4,5,8
| Maria Filomena Botelho
2,3,4,5
|
Eunice Virgínia Carrilho
1,2,3,4,5
1
Faculty of Medicine, Institute of Integrated
Clinical Practice, University of Coimbra,
Coimbra, Portugal
2
Faculty of Medicine, Coimbra Institute for
Clinical and Biomedical Research (iCBR),
University of Coimbra, Coimbra, Portugal
3
Center for Innovative Biomedicine and
Biotechnology, University of Coimbra,
Coimbra, Portugal
4
Faculty of Medicine, CIMAGO—Center of
Investigation on Environment, Genetics and
Oncobiology, University of Coimbra, Coimbra,
Portugal
5
CNC.IBILI, University of Coimbra, Coimbra,
Portugal
6
Faculty of Medicine, Laboratory of
Biostatistics and Medical Informatics,
University of Coimbra, Coimbra, Portugal
7
Faculty of Medicine, Experimental Pathology
Institute, University of Coimbra, Coimbra,
Portugal
8
Faculty of Medicine, Institute of Endodontics,
University of Coimbra, Coimbra, Portugal
Correspondence
Ana Sofia Coelho, Area de Medicina
Dentária—Av. Bissaya Barreto, Bloco de Celas,
3000-075 Coimbra, Portugal.
Email: anasofiacoelho@gmail.com
Abstract
Objective: To analyze articles aimed at evaluating the association between diabetes,
metabolic control, diabetes duration, and dental caries.
Overview: A systematic search in PubMed, Cochrane Library, Embase, and Web of
Science was conducted to retrieve papers in English, Portuguese, and Spanish, up to
April 2019. The research strategy was constructed considering the “PECO”strategy.
Only quantitative observational studies were analyzed. The risk of bias was assessed
using the Newcastle-Ottawa Quality Assessment Scale. The meta-analyses were per-
formed based on random-effects models using the statistical platform R. A total of
69 articles was included in the systematic review and 40 in the meta-analysis. Type
1 diabetics have a significantly higher DMFT compared to controls. No significant dif-
ferences were found between type 2 diabetics and controls and between well-
controlled and poorly controlled diabetics. Concerning diabetes duration, all authors
failed to find differences between groups.
Conclusion: Although there is still a need for longitudinal studies, the meta-analysis
proved that type 1 diabetics have a high dental caries risk.
Clinical significance: It is necessary to be aware of all risk factors for dental caries
that may be associated with these patients, making it possible to include them into
an individualized prevention program.
KEYWORDS
dental caries, diabetes mellitus, oral health
1|INTRODUCTION
Diabetes mellitus is presented as a set of metabolic disorders that are
characterized by hyperglycemia resulting from a deficiency in insulin
production and/or action. Chronic hyperglycemia results in a distur-
bance in the metabolism of carbohydrates, lipids, and proteins and in
numerous long-term complications that cause damage, dysfunction,
and failure of several organs.
1-3
Secondary complications resulting from a fluctuation in the blood
glucose levels are frequent and occur due to vascular degeneration in
different organs.
2
Despite advances in terms of diagnosis, prevention
and treatment, diabetic complications remain a major cause of mor-
bidity and mortality.
4-6
Type 1 diabetes mellitus includes the cases in which there is a
destruction of β-pancreatic cells by autoimmune processes (type 1A)
and those in which the etiology and pathogenesis of the destruction is
Received: 29 August 2019 Revised: 4 November 2019 Accepted: 17 December 2019
DOI: 10.1111/jerd.12562
J Esthet Restor Dent. 2020;1–19. wileyonlinelibrary.com/journal/jerd © 2020 Wiley Periodicals, Inc. 1

idiopathic (type 1B), which occurs less frequently. Type 2 diabetes
mellitus is characterized by insulin resistance and relative deficiency
of its secretion and it is often associated with obesity and metabolic
syndrome.
1,2,7-9
In 2013, a study by the International Diabetes Federation esti-
mated the global prevalence of patients with diabetes in 382 million,
predicting a prevalence of 592 million in 2035.
10
Although there are several oral complications associated with dia-
betic patients,
11,12
periodontal disease is the most frequently studied
one, being the other complications not adequately represented in
most studies.
Regarding dental caries, most studies include type 1 diabetic chil-
dren and the results are commonly controversial, which may be
explained by methodological differences between studies and the
multifactorial etiology associated with the disease.
The caries detection system proposed by the World Health Orga-
nization
13
remains the most widely used one in epidemiological stud-
ies aimed at assessing the prevalence of caries in different
populations and ages. DMF index is the total number of permanent
teeth or surfaces that are decayed (D), missing (M), or filled (F) due to
caries. When applied to teeth, the index is called DMFT and when
applied only to tooth surfaces it is called DMFS. The index can also be
applied to the primary dentition (dmft/dmfs, written in lowercase
letters).
The purpose of this study was to conduct a systematic review
and meta-analysis by analyzing articles aimed at evaluating the associ-
ation between diabetes mellitus, metabolic control, diabetes duration,
and dental caries. To this end, the authors formulated the following
questions:
1. When compared to non-diabetic healthy individuals, do patients
with diabetes mellitus have a higher prevalence of dental caries?
2. Do diabetics with a bad metabolic control have a higher prevalence
of dental caries when compared to diabetics with a good metabolic
control?
3. Do diabetics with a longer duration of the disease have a higher
prevalence of dental caries when compared to diabetics with a
shorter duration of the disease?
2|MATERIALS AND METHODS
This systematic review and meta-analysis protocol was registered
with the International Prospective Register of Systematic Reviews
(PROSPERO)—CRD42018092877. The Preferred Reporting Items for
Systematic Reviews and Meta-Analyses Protocols (PRISMA-P) were
followed.
14
An electronic search was performed using Cochrane Library
(www.cochranelibrary.com), Embase (www.embase.com), PubMed
(www.ncbi.nlm.nih.gov/pubmed) and Web of Science (www.
webofscience.com) through April 30, 2019 without any restrictions on
publication type, region or year. The search was limited to articles in
English, Spanish and Portuguese. The MeSH terms used were “dental
caries”,“oral health”and “diabetes mellitus.”Furthermore, MeSH syn-
onyms and related terms were included (Table 1). The reference lists
of relevant studies and reviews were manually searched for additional
reports. Google was used for to search for grey literature. When mul-
tiple articles describing the same population were found, the most
recent one was reported.
The research strategy was constructed considering the “PECO”
(Patient, Exposure, Comparison, Outcome) method.
15
The studies to
be included evaluated patients (P) with type 1 or with type 2 diabetes
mellitus (E) and a comparison group of non-diabetic healthy individuals
(C). The outcome (O)—prevalence of dental caries in the permanent or
primary dentition—should be reported according to the decayed, miss-
ing and filled (DMF/dmf) indices presented as means with SD.
Regarding the evaluation of the role of metabolic control and dia-
betes duration in dental caries, a comparison group of non-diabetic
individuals was not required.
Only quantitative observational studies on the association
between diabetes mellitus and dental caries were analyzed. Studies
evaluating patients with type 1 and type 2 diabetes together were
excluded, as well as studies whose authors only selected diabetic
patients with other diseases or according to their smoking habits and
articles on dental caries prevalence in newly diagnosed diabetic
patients. Review articles, nonhuman studies, letters, case reports, con-
ference abstracts and comments were also excluded.
The titles and abstracts retrieved were analyzed to identify
potentially eligible studies. All titles and abstracts were examined by
2 reviewers independently to find relevant studies. The full texts of
the relevant studies were scrutinized by the same two reviewers. Any
disagreement was discussed and the opinion of a third reviewer was
obtained when necessary.
TABLE 1 Search strategy for each database
Database Search strategy
Cochrane
Library
#1 MeSH descriptor: [Dental Caries] explode all trees
#2 carie*
#3 carious
#4 decay*
#5 MeSH descriptor: [Oral Health] explode all trees
#6 “oral health”
#7 #1 or #2 or #3 or #4 or #5 or #6
#8 MeSH descriptor: [Diabetes Mellitus] explode all
trees
#9 diabetes
#10 diabetic*
#11 #8 or #9 or #10
#12 #7 and #11
Embase (‘dental caries’/exp OR ‘carie*’OR decay*OR carious
OR ‘oral health’) AND (‘diabetes mellitus’/exp OR
‘diabetes’OR diabetic*)
Pubmed (((((((dental caries[MeSH Terms]) OR carie*) OR carious)
OR decay*) OR oral health[MeSH Terms]))) AND
(((diabetes mellitus[MeSH Terms]) OR diabetes) OR
diabetic*)
Web of
Science
TOPIC: (caries OR carious OR decay OR “oral health”)
AND TOPIC: (diabetes OR diabetic*)
2COELHO ET AL.

When needed, study authors were contacted in order to request
missing data and/or seek clarification.
For each included study, descriptive and quantitative information
was collected, including authors, country and year of publication, sam-
ple size, age of participants, diabetes type, criteria adopted to assess
the outcome, diabetes duration, metabolic control, results, and
limitations.
The meta-analyses, resulting from the systematic review, were
performed using the “metaphor”package accessible in the statistical
platform R (v.3.3.2). In order to consider the heterogeneity of the
studies, which was evaluated with the Q test and the I
2
statistic, the
meta-analyses were performed based on random-effects models. For
meta-analysis computation the difference in means from each individ-
ual study were used. Studies evaluating patients with type 1 diabetes
were analyzed in two groups according to the caries indices used by
the authors (dmft/DMFT). Only studies using the DMFT index were
included in the meta-analysis regarding type 2 diabetics. For the
meta-analysis of studies evaluating patients with controlled diabetes
and patients with uncontrolled diabetes a HbA
1c
cut-off of 7% was
considered since most diabetes mellitus treatment guidelines set a
maximum limit up to 7% for a good metabolic control for most
patients—for this analysis type 1 and type 2 diabetics were separately
evaluated.
The risk of bias of the studies included in the systematic review
and meta-analysis was assessed using the modified Newcastle-
Ottawa Quality Assessment Scale for cross-sectional studies
16
by two
independent reviewers. The methodological quality score was calcu-
lated based on three domains: Selection (0-4 points), Comparability
(0-2 points), and Exposure (0-3 points). To the assessment of each
domain, a series of multiple choice questions were answered by the
same two independent reviewers based on the reading and under-
standing of each study. A study can be awarded a maximum of one
point for each numbered item within the Selection (four items) and
Exposure (three items) domains and a maximum of two points can be
awarded for Comparability (two items). Therefore, the scores may
vary from 1 to a maximum of 9 points.
FIGURE 1 Flowchart of study
selection process
COELHO ET AL.3

TABLE 2 Dental caries prevalence (Type 1 diabetics)
Authors, year Subject N dmft dmfs dt mt ft dfs DMFT DT MT FT DMFS DFS DS MS FS
Geetha et al,
17
2019 DM1 175 *0.26 ± 0.05 *0.39 ± 0.08 *0±0 *0±0 *0.7 ± 0.45 *0.7 ± 0.4 *0.07 ± 0.006 *0.2 ± 0.06
Control 175 0.84 ± 0.2 0.73 ± 0.2 0.07 ± 0.01 0.07 ± 0.01 1.75 ± 0.8 1.46 ± 0.6 0.1 ± 0.01 0.43 ± 0.1
Kamran et al,
18
2019 DM1 100 2.6 ± 1.25
Control 100 2.52 ± 1.26
Shakra & Foqaha,
19
2019
DM1 60 2.5 ± 3 2.6 ± 3.3
Control 60 3.6 ± 3.4 1.2 ± 1.8
Babu et al,
21
2018 DM1 80 0.44 ± 1.28 *1.26 ± 2.49
Control 80 0.88 ± 1.75 0.46 ± 1.02
Coelho et al,
22
2018 DM1 60 1.72 ± 2.29 3.73 ± 4.79 *5.15 ± 3.95 *4.77 ± 6.07
Control 60 1.28 ± 1.76 2.9 ± 4.34 3.55 ± 3 2.56 ± 3.89
Coelho et al,
23
2018 DM1 36 0.22 ± 0.68 *0.08 ± 0.50 0.97 ± 1.65 1.47 ± 2.021
Control 36 0.36 ± 0.87 0.61 ± 1.18 1.08 ± 1.84 2.11 ± 2.35
Ferizi et al,
24
2018 DM1 80 *6.56 ± 3.56 4.78 ± 3.19 0.65 ± 1.42 1.14 ± 1.52
Control 80 4.21 ± 2.63 1.58 ± 1.9 0.75 ± 1.11 1.89 ± 1.65
Ambildhok et al,
20
2018 DM1 100 *3.66 ± 4.80 *6.55 ± 5.80
Control 200 1.22 ± 1.09 2.44 ± 2.12
Machado et al,
28
2018 DM1 30 3.83 ± 2.6 1.43 ± 4.22 2.73 ± 2.75
Control 30 4.73 ± 2.94 1.57 ± 3.71 2.07 ± 1.93
Techera et al,
25
2018 DM1 56 1.23 ± 1.977
Control 30 1.04 ± 1.88
Basir et al,
26
2017 DM1 27 *5.68 ± 1.13
Control 27 0.88 ± 0.16
Ismail et al,
27
2017 DM1 32 1.09 ± 2.43 0.53 ± 1.85 0.31 ± 1.00 0.25 ± 0.98 1.69 ± 1.75 0.56 ± 0.84 0 ± 0 1.13 ± 1.34
Control 32 1.38 ± 2.71 1.28 ± 2.54 0 ± 0 0.09 ± 0.3 2.03 ± 1.75 0.31 ± 0.59 0 ± 0 1.70 ± 1.46
Sadeghi et al,
29
2017 DM1 36 2.5 ± 2
Control 36 2.02 ± 1.7
Fazli
c et al,
30
2016 DM1 60 *11.49 ± 3.1 *5.27 ± 3.38 *1.47 ± 1.69 *4.75 ± 2.51
Control 30 6.19 ± 2.54 2.63 ± 2.61 0.43 ± 0.86 3.13 ± 2.83
Garcia et al,
31
2016 DM1 30 4.6 ± 4.26 4.23 ± 4.28 4.8 ± 3.15
Control 30 4.17 ± 3.09 3.42 ± 4.6 3.77 ± 3.22
Rafatjou et al,
32
2016 DM1 73 3.78 ± 3.24
Control 75 3.08 ± 2.74
Rafatjou et al,
32
2016 DM1 28 *2.52 ± 3.29
Control 33 5.36 ± 3.21
Busato et al,
33
2016 DM1 32 4 ± 0.7
Control 32 1 ± 0.3
(Continues)
4COELHO ET AL.

TABLE 2 (Continued)
Authors, year Subject N dmft dmfs dt mt ft dfs DMFT DT MT FT DMFS DFS DS MS FS
Singh-Hüsgen et al,
34
2016
DM1 100 *3.86 ± 7.68 3.08 ± 11.38
Control 100 1.38 ± 5.33 2.57 ± 7.11
Subramaniam et al,
35
2015
DM1 30 1.07 ± 2.43
Control 30 0.5 ± 1.14
Arheiam & Omar,
36
2014
DM1 70 1.19 ± 1.74 *0.91 ± 1.32 *0.19 ± 0.57 0.09 ± 0.33
Control 70 0.8 ± 1.46 0.57 ± 1.19 0.1 ± 0.35 0.1 ± 0.42
Gupta et al,
38
2014 DM1 140 0.59 ± 1.36 0.6 ± 1.63 2.09 ± 2 *1.91 ± 1.94 *0.047 ± 0.21 0.13 ± 0.38 2.25 ± 2.31 2.05 ± 2.18 0.19 ± 0.85 *0.02 ± 0.14
Control 140 0.77 ± 1.37 1.15 ± 1.91 2.25 ± 1.64 2.07 ± 1.6 0.04 ± 0.2 0.14 ± 0.45 2.74 ± 2.11 2.43 ± 1.99 0.16 ± 0.79 0.15 ± 0.47
Bassir et al,
37
2014 DM1 31 3.71 ± 2.48 2.41 ± 1.92 0.32 ± 0.54 0.96 ± 1.1
Control 31 4.35 ± 2.74 2.87 ± 1.12 0.32 ± 0.54 1.2 ± 1.13
Alves et al,
39
2012 DM1 51 0.64 ± 1.24 1.94 ± 2.84
Control 51 1.27 ± 2.42 1.41 ± 2.34
El-Tekeya et al,
41
2012 DM1 50 6.33 ± 4.48 0.82 ± 1.58
Control 50 5.81 ± 5 0.7 ± 1.26
Akpata et al,
40
2012 DM1 53 *6.4 ± 4.7 *3.7 ± 3.2 7.3 ± 6.5 1.4 ± 2.8 *3.8 ± 3.3
Control 53 4.7 ± 3.3 1.8 ± 2.3 5.6 ± 4 1 ± 1.5 2.1 ± 2.9
Tagelsir et al,
43
2011 DM1 52 2.86 ± 2.52 3.89 ± 3.81 3.84 ± 3.89 5.61 ± 5.97
Control 50 3.51 ± 2.76 7.03 ± 7.33 2.85 ± 2.47 4.46 ± 3.98
del Valle &
Oca-sio-Lopez,
62
2011
DM1 25 *1.43 ± 1.8
Control 25 0.56 ± 1
Busato et al,
45
2010 DM1 51 *3.3 ± 3.7
Control 51 1.5 ± 2.1
Miko et al,
44
2010 DM1 259 *11.15 ± 4.2 *3.89 ± 3.64 *3.9 ± 2.3 *3.36 ± 3.48
Control 259 9.56 ± 5.15 6.39 ± 3.95 3.89 ± 3.09 0.89 ± 1.5
Neil et al,
46
2009 DM1 63 0.09 ± 0.1
Control 63 0.2 ± 0.15
Vaziri et al,
47
2009 DM1 40 10.16 ± 4.52
Control 20 8.26 ± 3.85
Siudikiene et al,
49
2008 DM1 63 0.7 ± 1.9 5.79 ± 6.6 34.5 ± 16.6
Control 63 0.2 ± 1.4 6.2 ± 5.2 37.1 ± 15.1
Orbak et al,
48
2008 DM1 50 0.6 ± 1 *1.7 ± 2.1 *1.3 ± 1.9
Control 50 0.7 ± 1.1 5.5 ± 8.3 4.6 ± 7.7
Ilgüy & Bayirli,
50
2007 DM1 46 38.17 ± 29.88 4.36 ± 3.95 *23.04 ± 24.86 10.76 ± 12.74
Control 50 21.64 ± 20.36 3.36 ± 3.18 8.04 ± 9 10.24 ± 13.32
Amaral et al,
51
2006 DM1 30 *6.7 ± 5.7
Control 84 10.5 ± 5.8
(Continues)
COELHO ET AL.5

TABLE 2 (Continued)
Authors, year Subject N dmft dmfs dt mt ft dfs DMFT DT MT FT DMFS DFS DS MS FS
Siudikiene et al,
53
2006 DM1 68 0.29 ± 1.47 3.13 ± 3.74 *23.03 ± 14.54
Control 68 0.07 ± 0.61 3.97 ± 3.93 27.43 ± 16.04
Miralles et al,
52
2006 DM1 90 *7.41 ± 4.17
Control 90 5.63 ± 4.04
Edblad et al,
54
2001 DM1 41 7.3 ± 4.2 15.4 ± 10.4
Control 41 6.5 ± 4 12.1 ± 10.1
Moore et al,
55
2001 DM1 390 *2.51 ± 0.23 *33.7 ± 1.2 21.7 ± 0.8 1 ± 0.1
Control 202 1.44 ± 0.28 26.2 ± 1.7 19.1 ± 1.2 0.9 ± 0.2
Swanljung et al,
56
1992 DM1 85 4.3 ± 3.1 5.8 ± 5
Control 85 3.3 ± 2.7 4 ± 3.9
Akyuz & Oktay,
57
1990 DM1 42 *4.55 ± 2.45
Control 20 6.4 ± 2.7
Tenovuo et al,
59
1986 DM1 35 37.9 ± 25 *8.5 ± 12.4 *23.5 ± 16.1
Control 35 45.7 ± 24.5 3.4 ± 3.2 36.3 ± 15.8
Goteiner et al,
58
1986 DM1 169 4.53 ± 3.8
Control 80 4.46 ± 3.22
Bernick et al,
60
1975 DM1 50 8.27 ± 1.34
Control 36 8.89 ± 1
Matsson & Koch,
61
1975 DM1 33 *13.4 ± 1.6
Control 33 20.5 ± 2.6
Abbreviation: DM1, Type 1 Diabetes mellitus.
Note: Primary dentition—dmft, decayed, missing, and filled teeth; dt, decayed teeth; mt, missing teeth; ft, filled teeth; dmfs, decayed, missing, and filled surfaces; dfs, decayed and filled surfaces. Permanent
dentition—DMFT, decayed, missing, and filled teeth; DT, decayed teeth; MT, missing teeth; FT, filled teeth; DMFS, decayed, missing, and filled surfaces; DFS, decayed and filled surfaces; DS, decayed surfaces;
MS, missing surfaces; FS, filled surfaces.
*Statistically significant difference (P< 0.05).
6COELHO ET AL.

TABLE 3 Dental caries prevalence (Type 2 diabetics)
Authors, year Subject N DMFT DT MT FT DMFS DFS DS MS FS DR DRS FRS
Arab & Keshavarzi,
63
2018 DM2 50 *32.4 ± 1.5
Control 50 25.0 ± 1.5
Latti et al,
64
2018 DM2 30 *10.67 ± 5.2
Control 30 5.6 ± 2.59
Puttaswamy et al,
65
2017 DM2 60 5.75 ± 3.53
Control 40 5.83 ± 4.11
Malvania et al,
66
2016 DM2 120 *2.43 ± 2.88 1.06 ± 0.58 *1.24 ± 0.91 0.1 ± 0.47
Control 120 0.74 ± 1.27 0.46 ± 1.03 0.23 ± 0.63 0.07 ± 0.36
Singh et al,
67
2016 DM2 30 *14.8 ± 0.59
Control 30 3.75 ± 0.24
Lima et al,
68
2014 DM2 50 *30.7 ± 3.6 0.1 ± 0.4 29.8 ± 6.1 0.8 ± 2.7
Control 50 22.3 ± 4.6 1.5 ± 1.6 17.9 ± 6.8 2.9 ± 3.1
Singh et al,
69
2014 DM2 60 *12.6 ± 0.48
Control 60 2.67 ± 0.14
Sukminingrum et al,
70
2013 DM2 23 *13.52 ± 3.69 *6.7 ± 2.067
Control 26 9.73 ± 2.50 3.81 ± 1.772
Aziz et al,
71
2012 DM2 180 14.04 ± 7.06 2.1 ± 1.46 *10.84 ± 7.27 *1.03 ± 1.37
Control 180 12.65 ± 8.22 1.93 ± 1.63 9.17 ± 6.32 1.47 ± 1.56
Vaziri et al,
47
2009 DM2 40 13.42 ± 5.09
Control 21 10.55 ± 2.59
Marín et al,
72
2008 DM2 35 19.6 ± 3.9 10.5 ± 6 *5.7 ± 3.7 3.4 ± 3.7
Control 35 18.2 ± 3.5 10.9 ± 6.1 3.5 ± 2.9 3.7 ± 3.7
Hintao et al,
78
2007 DM2 105 3.8 ± 0.2 8 ± 9.4 *1 ± 0.2 *1.2 ± 0.2
Control 103 3.3 ± 0.3 6.3 ± 7.5 0.4 ± 0.1 0.5 ± 0.1
Ilgüy & Bayirli,
50
2007 DM2 40 46.42 ± 32.33 3.35 ± 3.4 *32.4 ± 27.31 10.85 ± 13.56
Control 50 21.64 ± 20.36 3.36 ± 3.18 8.04 ± 9 10.24 ± 13.32
Zielinski et al,
74
2002 DM2 32 8.9 ± 6.1 9.2 ± 6.6
Control 40 9.3 ± 6.7 9.1 ± 6.2
Lin et al,
75
1999 DM2 24 *41.3 ± 20.9 1.8 ± 2.6 *56 ± 34.1 *39.5 ± 20.5 1.3 ± 1.8 *14.5 ± 15.8
Control 18 54.9 ± 20.3 1 ± 1 38.1 ± 28.1 53.9 ± 20.2 0.6 ± 1 24.1 ± 13.3
Collin et al,
76
1998 DM2 25 23.8 ± 6
Control 40 25.1 ± 4.3
Cherry-Peppers & Ship,
77
1993 DM2 11 53.8 ± 29.7 *3.8 ± 9.5 20.3 ± 19.6 30 ± 13
Control 43 56.9 ± 33.9 0.7 ± 1.7 16.9 ± 26.8 37 ± 21.6
Abbreviations: DMFT, decayed, missing, and filled teeth; DT, decayed teeth; MT, missing teeth; FT, filled teeth; DMFS, decayed, missing, and filled surfaces; DFS, decayed and filled surfaces; DS, decayed
surfaces; MS, missing surfaces; FS, filled surfaces; DR, decayed roots; DRS, decayed root surfaces; FRS, filled root surfaces; DM2, Type 2 Diabetes mellitus.
*Statistically significant difference (P< .05).
COELHO ET AL.7

TABLE 4 Dental caries and metabolic control
Authors, year
N
HbA
1c
(%) dfs dmft dmfs DMFT DFT DT MT FT DMFS DFS DS MS FSDM1 DM2
Kamran et al,
18
2019 30 <7 2.63 ± 1.11
15 ≤7 to <8 2.33 ± 1.11
55 ≥8 2.65 ± 1.27
Vidya et al,
80
2018 19 <7 *0.16 ± 0.38
68 >7 1.47 ± 2.77
Sadeghi et al,
29
2017 9 ≤7 2.3 ± 0.7 3.1 ± 0.9
21 >7 to ≤8 2.5 ± 0.5 2.7 ± 0.4
20 >8 0.5 ± 0.3 3.2 ± 0.5
Fazli
c et al,
30
2016 30 ≤7 10.57 ± 3.22
30 >7 12.39 ± 2.97
Kogawa et al,
81
2016 32 <7 20.25 ± 6.7
31 >7 18.23 ± 7.31
Malvania et al,
66
2016 47 ≤7*0.62 ± 1.01 0.36 ± 0.79 *0.32
± 0.66
0.04 ± 0.2
73 >7 3.46 ± 3.16 1.51 ± 1.8 1.83 ± 2.2 0.14
± 0.58
Karthikeyan et al,
82
2015
25 ≤7*18.16 ± 9.57 *14.08
± 7.59
1.2 ± 2.61 3.28 ± 3.51
25 >7 37.76 ± 16.83 31.44
± 16.95
2 ± 4.33 4.32 ± 5.76
Aziz et al,
71
2012 119 ≤7 13.92 ± 7.74
61 >7 14.28 ± 5.59
El-Tekeya et al,
41
2012 23 <8.5 7.09
± 5.09
0.78 ± 1.52
20 ≥9to
<10.5
5.63
± 3.73
0.78 ± 1.66
7≥11 5.86 ± 4.6 1.25 ± 1.89
Tagelsir et al,
43
2011 20 <7.5 2.75
± 1.98
3.93
± 3.54
3.16 ± 3.5 5 ± 6.76
22 ≥7.5 to
<8.5
3.39
± 2.88
5.31
± 4.09
4.18 ± 4.49 6.12 ± 5.94
10 ≥8.5 0.57
± 0.53
0.57
± 0.53
4.75 ± 3.45 6 ± 4.41
Busato et al,
62
2010 17 ≤8 3.6 ± 3.7 0.5 ± 1.2 0.5 ± 1.1 3.3 ± 4
34 >8 3.2 ± 3.7 0.3 ± 1 0.1 ± 0.5 2.9 ± 3.5
Miko et al,
44
2010 210 ≤6.5 12.91 ± 5.64 *3.48
± 2.22
4.98 ± 2.23 *4.46
± 2.1
49 >6.5 13.29 ± 3.25 5.98 ± 4.52 4.86 ± 1.69 2.45
± 1.16
(Continues)
8COELHO ET AL.

TABLE 4 (Continued)
Authors, year
N
HbA
1c
(%) dfs dmft dmfs DMFT DFT DT MT FT DMFS DFS DS MS FSDM1 DM2
Marín et al,
72
2008 35 ≤7 8.8 ± 4.8 5.5 ± 4.8 1.3 ± 2.2 1.9 ± 4.6
35 >7 8.6 ± 5.9 4.1 ± 4 2 ± 3.2 2.5 ± 3.8
Siudikiene et al,
53
2006 39 < 9 *19.51
± 12.62
0 ± 0 3.46 ± 4.17
29 ≥9 27.76 ± 15.78 0.69
± 2.21
2.69 ± 3.07
Miralles et al,
52
2006 46 ≤7.5 7.84 ± 4.48
44 >7.5 7.47 ± 4.29
Bolgül et al,
83
2004 15 <10 *2.2 ± 1.7
30 ≥10 to <13 4.1 ± 1.9
25 ≥13 7.1 ± 2.4
Syrjälä et al,
84
2003 69 ≤8.5 6.49 ± 6.25 24.91
± 18.15
59 >8 6.31 ± 6.75 23.05
± 19.92
Twetman et al,
85
2002 37 ≤8 0.6
± 1.1
*1.6 ± 2 *1.4 ± 1.9
27 >8 0.8
± 2.7
5.4 ± 8.4 4.8 ± 7.8
Edblad et al,
54
2001 26 <8 10.5
± 5.1
7.1 ± 4.1 16 ± 9.8
15 >8 9.6 ± 5 7.6 ± 4.4 14.5
± 11.7
Lin et al,
75
1999 9 ≤9 48.8
± 17.8
1.3 ± 2.1 41.6
± 25.9
47.4 ± 16.9
15 >9 36.9
± 21.9
2.1 ± 2.9 64.7
± 36.3
34.8 ± 21.4
Karjalainen et al,
86
1997 21 <10 *4.1 ± 6.9 0.2 ± 0.6 *3.9 ± 6.9
25 ≥10 to <13 2.3 ± 3.3 0.3 ± 0.7 2 ± 3.1
34 ≥13 7.5 ± 9.2 0.7 ± 1.8 6.9 ± 8.5
Harrison & Bowen,
87
1987
14 ≤10 4.8 ± 1.3
16 >10 5.6 ± 1.3
Abbreviations: DM1, Type 1 Diabetes mellitus; DM2, Type 2 Diabetes mellitus.
Note: Primary dentition: dmft, decayed, missing, and filled teeth; dfs, decayed and filled surfaces; dmfs, decayed, missing, and filled surfaces. Permanent dentition: DMFT, decayed, missing, and filled teeth; DFT,
decayed and filled teeth; DT, decayed teeth; MT, missing teeth; FT, filled teeth; DMFS, decayed, missing and filled surfaces; DFS, decayed and filled surfaces; DS, decayed surfaces; MS, missing surfaces; FS,
filled surface.
*Statistically significant difference (P< .05).
COELHO ET AL.9

TABLE 6 Risk of bias of the studies included in the systematic review and meta-analysis using the modified Newcastle-Ottawa Quality
Assessment Scale for cross-sectional studies
72
Authors, year Selection (0-4) Comparability (0-2) Exposure (0-3) Risk of bias (0–9)
Geetha et al,
17
2019 3 1 3 7
Kamran et al,
18
2019 2 1 3 6
Shakra et al,
19
2019 3 1 3 7
Ambildhok et al,
20
2018 3 1 3 7
Arab et al,
63
2018 2 1 3 6
Babu et al,
21
2018 3 1 3 7
Coelho et al,
22
2018 4 1 3 8
Coelho et al,
23
2018 3 1 3 7
Ferizi et al,
24
2018 3 1 3 7
Latti et al,
64
2018 2 2 3 7
Techera et al,
25
2018 3 1 3 7
Vidya et al,
80
2018 3 1 3 7
Basir et al,
26
2017 4 1 3 8
Ismail et al,
27
2017 3 1 3 7
Machado et al,
28
2017 3 1 3 7
Puttaswamy et al,
65
2017 2 2 3 7
Sadeghi et al,
29
2017 4 1 3 8
Busato et al,
33
2016 4 1 3 8
Fazli
c et al,
30
2016 3 1 3 7
Garcia et al,
31
2016 4 1 3 8
Kogawa et al,
81
2016 4 2 3 9
Malvania et al,
66
2016 2 1 3 6
Rafatjou et al,
32
2016 4 1 3 8
Singh et al,
67
2016 3 1 3 7
(Continues)
TABLE 5 Dental caries and diabetes duration
Authors, year
N
Duration (years) dmfs DMFT DT MT FT DMFSDM1 DM2
Kamran et al,
18
2019 48 <6 2.52 ± 1.11
52 ≥6 2.67 ± 1.38
Malvania et al,
66
2016 52 <2 2.05 ± 2.94 0.94 ± 1.43 1.02 ± 1.96 0.12 ± 0.58
17 2–5 2.69 ± 1.54 *0.5 ± 0.73 *1 ± 0.55 *0.12 ± 0.5
51 >5 3.01 ± 3.06 1.37 ± 1.87 1.57 ± 1.96 0.08 ± 0.33
Twetman et al,
88
1992 26 Onset 3.5 ± 6.1 3.1 ± 3.8
1 4 ± 6.6 4 ± 4.8
2 4 ± 6.6 4.1 ± 5.2
Miralles et al,
52
2016 39 <10 6.82 ± 3.9
51 >10 7.87 ± 4.19
Siudikiene et al,
49
2008 63 Baseline 0.3 ± 1.5 3.1 ± 4.4 23 ± 15
63 2 0.7 ± 1.9 5.79 ± 6.6 34.5 ± 17
Abbreviations: DM1, Type 1 Diabetes mellitus; DM2, Type 2 Diabetes mellitus.
Note: Primary dentition—dmfs: decayed, missing, and filled surfaces. Permanent dentition—DMFT, decayed, missing and filled teeth; DT, decayed teeth;
MT, missing teeth; FT, filled teeth; DMFS, decayed, missing and filled surfaces.
*Statistically significant difference (P< .05).
10 COELHO ET AL.

TABLE 6 (Continued)
Authors, year Selection (0-4) Comparability (0-2) Exposure (0-3) Risk of bias (0–9)
Singh-Husgen et al,
34
2016 3 1 3 7
Karthikeyan et al,
82
2015 4 1 3 8
Subramaniam et al,
35
2015 4 1 3 8
Arheiam et al,
36
2014 3 1 3 7
Bassir et al,
37
2014 4 1 3 8
Gupta et al,
38
2014 4 2 3 9
Lima et al,
68
2014 2 1 3 6
Singh et al,
69
2014 3 1 3 7
Sukminingrum et al,
70
2013 4 1 3 8
Akpata et al,
40
2012 4 2 3 9
Alves et al,
39
2012 2 1 3 6
Aziz et al,
71
2012 3 1 3 7
El-Tekeya et al,
41
2012 4 2 3 9
López del Valle & Ocasio-Lopez,
42
2011 3 1 3 7
Tagelsir et al,
43
2011 3 1 3 7
Busato et al,
45
2010 4 1 3 8
Miko et al,
44
2010 2 1 3 6
Neil et al,
46
2009 4 1 3 8
Vaziri et al,
47
2009 3 2 3 8
Marín et al,
72
2008 3 1 3 7
Orbak et al,
48
2008 2 1 3 6
Siudikiene et al,
49
2008 4 1 3 8
Hintao et al,
78
2007 3 2 3 8
Ilguy et al,
50
2007 3 1 3 7
Amaral et al,
51
2006 4 1 3 8
Miralles et al,
52
2006 3 1 3 7
Siudikiene et al,
53
2006 4 1 3 8
Bolgul et al,
83
2004 3 1 3 7
Syrjala et al,
84
2003 3 1 3 7
Twetman et al,
85
2002 3 1 3 7
Zielinski et al,
74
2002 3 1 3 7
Edblad et al,
54
2001 4 2 3 9
Moore et al,
55
2001 3 1 3 7
Lin et al,
75
1999 4 1 3 8
Collin et al,
76
1998 4 1 3 8
Karjalainen et al,
86
1997 3 2 3 8
Cherry-Peppers et al,
77
1993 4 1 3 8
Swanljung et al,
56
1992 3 2 3 8
Twetman et al,
88
1992 3 2 3 8
Akyuz & Oktay,
57
1990 3 1 3 7
Harrison et al,
87
1987 2 1 3 6
Goteiner et al,
58
1986 4 2 3 9
Tenovuo et al,
59
1986 2 2 3 7
Bernick et al,
60
1975 2 1 3 6
Matsson et al,
61
1975 3 1 3 7
COELHO ET AL.11

3|RESULTS
The flowchart of the study selection process is presented in Figure 1.
The literature search resulted in a total of 2744 unique articles, of
which 169 proceeded for examination of the full-text (2575 were
excluded). Eight additional studies were included for analysis from the
reference lists and grey literature. A hundred articles were excluded
since their authors did not report DMF indices, did not mention the
existence of a control group, used a special population (diabetic
patients with other diseases, smokers, or newly diagnosed) or did not
report the data as mean and SD.
Final analysis was carried out on 69 articles. Forty were pooled
for meta-analysis.
Forty-five articles
17-61
regarding caries experience among type 1 dia-
betics were analyzed (Table 2). Regarding type 2 diabetes 17 stud-
ies
47,50,63-77
were included (Table 3). Vaziri et al
79
and Ilgüy et al
50
evaluated type 1 and type 2 diabetics but results for each group were
separately reported. Twenty-two articles
18,29,30,41,43-45,52-54,66,71,72,75,80-87
regarding metabolic control and five
18,49,52,66,88
regarding diabetes
duration as a risk factor for dental caries were also analyzed (Tables 4 and
5, respectively).
The earliest studies were published in 1975 (Bernick et al
60
and
Matsson & Koch
61
) and the most recent ones were published in 2019
(Geetha et al,
17
Kamran et al,
18
and Shakra & Foqaha
19
).
Twelve of the studies were conducted in India,
17,20,21,35,38,64-67,69,80,82
eight in the United States,
42,55,58,60,74,75,77,87
six in Brazil,
33,39,45,51,68,81
five
in Finland,
56,59,76,84,86
four each in Portugal,
22,23,28,31
Sweden,
54,61,85,88
and
Turkey,
48,50,57,83
two in Lithuania,
49,53
oneeachinBelgium,
43
Bosnia and
Herzegovina,
30
China,
27
Egypt,
41
Germany,
34
Hungary,
44
Iraq,
71
Jordan,
19
Republic of Kosovo,
24
Kuwait,
40
Libya,
36
Malaysia,
70
Mexico,
72
Spain,
52
Sudan,
46
Thailand,
73
and Uruguay.
25
The majority of the studies regarding type 1 diabetes only
included children.
17-21,23-27,29,30,32-46,48,49,53,56-58,60,61
In most studies,
the control group was recruited from schools or dental clinics. Dia-
betic groups were often recruited from hospitals.
Intra-examiner agreement was stated in 15 studies and the kappa co-
efficient was between 0.70 and 0.97.
17,21,25,27,38,40,43,49,53,56,66,72,82,84,85
The inter-examiner agreement was stated in six studies and the kappa co-
FIGURE 2 Forest plot of meta-analysis for studies evaluating the DMFT in permanent dentition comparing patients with type 1 diabetes
mellitus (DM1) and controls
12 COELHO ET AL.

efficient was mainly over 0.80.
43,49,53,55,72
The lowest inter-examiner
agreement was reported by Lin et al
75
with a kappa co-efficient of 0.65.
The results of the studies' quality assessment are presented in
Table 6. The scores assigned range from 6 points (nine studies),
7 points (31 studies), 8 points (22 studies), and 9 points (six studies).
3.1 |Type 1 diabetes
Eleven studies
20,21,24,26,30,3 3,40,44,45,52,55
reported a DMFT/DMFS index
significantly higher among type 1 diabetics, four
17,38,53,57
found a sig-
nificantly lower index and 20
18,19,25,27,32,34-37,39,41,43,46,47,49,50,56,58-60
did not find statistically significant differences between groups.
Regarding dmft/dmfs index, Ambildhok et al
20
and Singh-Hüsgen
et al
34
reported a significantly higher index among type 1 diabetics
while Geetha et al,
17
Rafatjou et al,
32
Gupta et al,
38
and Amaral et al
89
reported a significantly lower index. Six studies
19,21,27,29,39,43
found
no statistically significant differences between groups.
In the meta-analysis, type 1 diabetic patients had a significantly
higher DMFT index than that of non-diabetic individuals (mean differ-
ence = −0.55; 95% CI: −1.10, −0.01, Figure 2). Significant
heterogeneity among studies was observed (I
2
= 98.5%; Q
[26] = 562.12; P< .001). Regarding dmft index no statistically signifi-
cant differences between groups were found (mean difference = 0.53;
95% CI: −0.20, 1.26, Figure 3) and a significant heterogeneity among
studies was observed (I
2
= 97.8%; Q[10] = 489.82; P< .001).
3.2 |Type 2 diabetes
Seven studies
63,64,66-70
reported a significantly higher DMFT index
among type 2 diabetics, while Lin et al
75
reported opposite results
regarding DFS. Seven studies
47,50,65,71,72,76,77
found no statistically
significant differences between groups.
Hintao et al
78
did not find significant differences between groups
regarding coronal caries. However, the authors reported a significant
higher prevalence of decayed roots among type 2 diabetics. Lin et al
75
reported opposite results regarding filled root surfaces.
No statistically significant differences were found between type 2 dia-
betics and controls regarding DMFT index (mean difference = −5.16;
95% CI: −10.62, 0.30, Figure 4). Significant heterogeneity among studies
was observed (I
2
= 99.9%; Q[11] = 609.28; P< .001).
FIGURE 3 Forest plot of meta-analysis for studies evaluating the dmft in temporary dentition comparing patients with type 1 diabetes
mellitus (DM1) and controls
COELHO ET AL.13

3.3 |Metabolic control
Siudikiene et al
53
found that the mean DMFS index of poorly con-
trolled (HbA
1c
≥9%) type 1 diabetic children was significantly higher
than that of well-controlled children (HbA
1c
< 9%). Bolgül et al
83
and
Karjalainen et al
86
reported similar DMFT/DFS results between poorly
(HbA
1c
≥13%), moderately (HbA
1c
≥10 to <13%) and well-controlled
(HbA
1c
< 10%) patients. Vidya et al
80
also reported a significantly
higher mean DMFT/DMFS indices of poorly controlled type 1 dia-
betics (HbA
1c
≥7%) compared to that of well-controlled patients
(HbA
1c
< 7%).
Twetman et al
85
observed type 1 diabetic children over a period
of 3 years and reported that HbA
1c
was higher in children who devel-
oped dental caries during the study period.
Concerning the meta-analysis only studies considering a HbA
1c
cut-off of 7% were used. No statistically significant differences were
found between well-controlled and poorly controlled type 1 diabetics
(mean difference = −0.34; 95% CI: −0.74, 0.06, Figure 5). No
heterogeneity among studies was observed (I
2
= 47.8%; Q
[2] = 3.82; P= .15).
Regarding type 2 diabetes mellitus, only five articles
66,71,75,81,82
reported results on the influence of metabolic control on dental caries
prevalence. Although Malvania et al
66
and Karthikeyan et al
82
reported a significantly higher DMFT/DMFS indices of poorly con-
trolled diabetics (HbA
1c
≥7%) compared to well-controlled
(HbA
1c
< 7%) diabetics, the meta-analysis did not find statistically sig-
nificant differences between well-controlled and poorly controlled
type 2 diabetics (mean difference = −0.30; 95% CI: −1.11, 0.52,
Figure 6). No heterogeneity among studies was observed (I
2
= 92.3%;
Q[2] = 24.10; P< .001).
3.4 |Diabetes duration
Although five articles
18,49,52,66,88
reported results on diabetes dura-
tion, all of them used different cut-off years. Regarding DMFT index,
all authors failed to find statistically significant differences between
groups.
The results regarding the prevalence of dental caries as well as the
weight of the different risk factors associated with diabetic patients are
FIGURE 4 Forest plot of meta-analysis for studies evaluating the DMFT in permanent dentition comparing patients with type 2 diabetes
mellitus (DM1) and controls
14 COELHO ET AL.

controversial. The meta-analysis revealed a statistically significant dif-
ference between type 1 diabetics and control individuals. However, it
failed to prove these differences regarding type 2 diabetics. A higher
risk of root caries is described for type 2 diabetics, which may be
related to the increasing susceptibility to periodontal disease, but few
studies aimed at evaluating this condition.
44,76,78,90
FIGURE 5 Forest plot of meta-analysis for studies evaluating the DMFT in permanent dentition comparing patients with controlled type
1 diabetes (HbA
1c
≤7) and patients with uncontrolled type 1 diabetes (HbA
1c
>7)
FIGURE 6 Forest plot of meta-analysis for studies evaluating the DMFT in permanent dentition comparing patients with controlled type
2 diabetes (HbA
1c
≤7) and patients with uncontrolled type 2 diabetes (HbA
1c
>7)
COELHO ET AL.15

4|DISCUSSION
Studies evaluating patients with type 1 and type 2 diabetes together
were excluded from this review. Although a large number of risk fac-
tors are common to these two types of patients, the higher prevalence
of periodontal disease associated with type 2 diabetics, the differ-
ences in dietary habits, as well as the different medical complications
associated with them, for example, can make it difficult to interpret
the results.
37,89,91
Singh-Hüsgen et al
34
developed a study that included 100 diabetic
children and 100 sex-age-matched controls and found no statistically
significant differences between groups regarding dental caries. The
authors associated the results with the metabolic control of the dia-
betics, since 88% of the sample was considered to be metabolically
well-controlled. However, in cross-sectional studies, Kamran et al,
18
Sadeghi et al,
29
El-Tekeya et al,
41
and Tagelsir et al
43
found no signifi-
cant differences regarding dental caries between metabolically well,
moderately, and poorly controlled. The evaluation of the effect of the
metabolic control in the development of dental caries may, however,
be better evaluated in longitudinal studies since HbA
1c
levels fluctu-
ates in diabetics.
Although in the meta-analysis no statistically significant differ-
ences were found concerning metabolic control for type 1 and 2 dia-
betics, it should be taking into account that only a HbA
1c
cut-off of
7% was considered. The heterogeneity regarding the cut-offs of the
studies evaluating the metabolic control made it impossible to include
more studies in the meta-analysis. Also, this large variety of cut-offs
makes it very difficult to interpret the results.
Twetman et al
85,92
conducted a longitudinal study and found a
positive correlation between the risk of caries when diabetes was
diagnosed and metabolic control 3 years after the initial observation.
However, this correlation may reflect mainly the importance of behav-
ioral factors in the sense that a greater concern for oral health can be
included in a general health awareness and thus, be associated with a
greater commitment to diabetes treatment.
The heterogeneity regarding the cut-offs of the studies evaluating
the diabetes duration made it impossible to conduct a meta-analysis.
Although no statistically significant differences between long and
short diabetes duration was found, that was expected since there are
known biological and behavioral changes over the time. In fact, diabe-
tes duration is associated with micro and macrovascular
complications.
93-95
The highest risk of bias, resulting in the lowest scores, was identi-
fied in the first domain—Selection—more precisely in items number
2 (Representativeness of the cases) and 3 (Selection of Controls). In
item number 2, 15 studies were identified as having insufficient/non-
existent description regarding the selection process of the groups,
making no reference to possible confounding factors and lacking well-
defined inclusion and exclusion criteria. The non-parametrization of
the criteria and the insufficient information provided by the studies
makes it impossible to reproduce them and to confirm the homogene-
ity of the groups. In item number 3, 18 studies described the selection
process of the control group as being from public and private hospitals
and dental clinics. This might be considered a possible bias since the
individuals selected from these establishments are neither representa-
tive of a randomized group nor of the general community. In addition
to these studies, 14 others do not make any description about the ori-
gin of the recruitment of the controls, not providing sufficient infor-
mation for the evaluation and validation of these groups.
Regarding the remaining items and domains, all of them presented
a low risk of bias, since all the studies had an adequate definition—
with independent validation—and all individuals of the control groups
had no history of disease (diabetes) in all phases of the studies. All
records and results were considered safe and reliable and it is com-
mon to all studies that the methods used to evaluate the established
study parameters were the same for both test and control groups.
Diabetic patients have inherently associated several risk factors
for the development of dental caries. The greater number of daily
meals to which these patients are subjected, consequently, translates
into a greater daily supply of nutrients that influence the proliferation
of microorganisms in the oral cavity as well as the maintenance of a
lower salivary pH, a risk factor for the development of dental car-
ies.
37,89,96,97
Salivary pH has been studied and proven to reach lower
values in diabetic patients compared to healthy individuals.
98,99
Sev-
eral factors contribute to this decrease: the low concentration of
bicarbonate, the greater accumulation of dental plaque and saliva with
high cariogenic load and an increased concentration of salivary glu-
cose, possibly related to microvascular complications (damage to the
basal membrane of salivary glands leads to an endothelial dysfunction
and the glucose molecule is easily released to the existing
saliva).
22,100-103
Given the heterogeneity of the diabetic population and the differ-
ent risk factors that exist, a dietary assessment is also extremely impor-
tant as it allows analyzing the frequency of ingestion of cariogenic
products—high or low—enabling the identification of this parameter as
a risk or protective factor, respectively. Diabetic patients who present
better dietary habits, such as reduced intake of cariogenic products, are
those who have a better nutritional control and who are motivated and
willing to cooperate towards a healthier lifestyle.
37,89,96,97
The resolution of hypoglycemic episodes using sugar requires the
diabetic patient to be well informed about procedures for proper oral
cavity hygiene, especially when these episodes occur at night.
Decreased salivary flow is very common in diabetic patients, espe-
cially at night. This decrease leads to reduced substrate elimination
and decreased sugar dissolution rates, leading to less effective pH reg-
ulation and antimicrobial mechanisms, promoting bacterial prolifera-
tion and sugar metabolization by cariogenic bacteria. All this may also
lead to demineralization of the dental structure.
98,99
Dental caries is a multifactorial condition and, as such, implies a
thorough and careful assessment of all its etiological factors so that it
is possible to assess the risk profile of each diabetic patient. Assess-
ment of primary—carbohydrate consumption and presence of cario-
genic microorganisms—and secondary factors—oral hygiene habits—is
required.
62,104,105
Most studies do not make this multifactorial assessment, not con-
sidering many other factors, making it very difficult to accurately
16 COELHO ET AL.

assess the results. On the other hand, a result demonstrating the exis-
tence of an association does not necessarily imply the existence of a
causal relationship. Therefore, it is necessary to be aware of all risk
factors for dental caries that may be associated with diabetic patients,
so that, after analysis, it is possible to include the patient into an
appropriate control and prevention program, taking into consideration
their risk profile.
Although the effect of diabetes mellitus on the prevalence of den-
tal caries has been the subject of study, the effects of metabolic con-
trol and lifestyle changes make it difficult to review. Moreover, most
studies differ in sample size (which is often reduced) and the meta-
bolic control, the medication and the presence of other oral patholo-
gies are not always considered.
5|CONCLUSIONS
Type 1 diabetics have a high dental caries risk. It is necessary to be
aware of all risk factors for dental caries that may be associated with
these patients, making it possible and safe to include the patient into
an appropriate and individualized control and prevention program,
taking into consideration their risk profile.
Although no correlation was found between metabolic control,
diabetes duration and dental caries, the importance of the behavioral
factors as well as the systemic complications associated with these
patients cannot be underestimated.
DISCLOSURE STATEMENT
The authors do not have any financial interest in the companies
whose materials are included in this article.
CONFLICT OF INTEREST
No conflicts of interest.
ORCID
Ana Sofia Coelho https://orcid.org/0000-0002-2924-7926
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How to cite this article: Coelho AS, Amaro IF, Caramelo F,
et al. Dental caries, diabetes mellitus, metabolic control and
diabetes duration: A systematic review and meta-analysis. J
Esthet Restor Dent. 2020;1–19. https://doi.org/10.1111/jerd.
12562
COELHO ET AL.19