Table Of ContentRAPID COMMUNICATION
Can fasting plasma glucose and glycated hemoglobin
levels predict oral complications following invasive
dental procedures in patients with type 2 diabetes
mellitus? A preliminary case-control study
AnaCarolinaFragosoMotta,ICristianeAparecidaNogueiraBataglion,IMariaCristinaFoss-Freitas,IIMilton
Cesar Foss,II Marilena Chinali KomesuI
IUniversityofSa˜oPaulo,DentalSchoolofRibeira˜oPreto,DepartmentofMorphology,StomatologyandPhysiology,Ribeira˜oPreto/SP,Brazil.IIUniversity
Sa˜oPaulo,SchoolofMedicineofRibeira˜oPreto,DepartmentofInternalMedicine,DivisionofEndocrinologyandMetabolism,Ribeira˜oPreto/SP,Brazil.
OBJECTIVE:Toevaluatetheeffectsofthelevelsofglycemiccontrolonthefrequencyofclinicalcomplications
followinginvasivedentaltreatmentsintype2diabeticpatientsandsuggestappropriatelevelsoffastingblood
glucose andglycated hemoglobin considered to besafeto avoid these complications.
METHOD:Type2diabeticpatientsandnon-diabeticpatientswereselectedanddividedintothreegroups.GroupI
consistedof13type2diabeticpatientswithadequateglycemiccontrol(fastingbloodglucoselevels,140mg/dl
andglycatedhemoglobin(HbA1c)levels,7%).GroupIIconsistedof15type2diabeticpatientswithinadequate
glycemiccontrol(fastingbloodglucoselevels.140mg/dlandHbA1clevels.7%).GroupIIIconsistedof18non-
diabeticpatients(nosymptomsandfastingbloodglucoselevels,100mg/dl).Thelevelsoffastingbloodglucose,
glycatedHbA1c,andfingerstickcapillaryglycemiawereevaluatedindiabeticpatientspriortoperformingdental
procedures.Sevendaysafterthedentalprocedure,thefrequencyofclinicalcomplications(surgerysiteinfections
andsystemicinfections)wasexaminedandcomparedbetweenthethreestudygroups.Inaddition,correlations
betweentheoccurrenceoftheseoutcomesandtheglycemiccontrolofdiabetesmellituswereevaluated.
RESULTS:Thefrequencyofclinicaloutcomeswaslow(4/43;8.6%),andnosignificantdifferencesbetweenthe
outcomefrequenciesofthevariousstudygroupswereobserved(p.0.05).However,asignificantassociationwas
observedbetweenclinicalcomplicationsanddentalextractions(p=0.02).
CONCLUSIONS: Because of the low frequency of clinical outcomes, it was not possible to determine whether
fastingbloodglucoseorglycatedHbA1clevelsareimportantfortheseclinicaloutcomes.
KEYWORDS: Type2DiabetesMellitus;OralInfections;GlycemicControl.
Motta AC, Bataglion CA, Foss-Freitas MC, Foss MC, Komesu MC. Can fasting plasma glucose and glycated hemoglobin levels predict oral
complications following invasive dental procedures in patients with type 2 diabetes mellitus? A preliminary case-control study. Clinics.
2013;68(3):427-430.
E-mail:[email protected]
Tel.:55163602-4109
& INTRODUCTION glucose (4). It has been reported that chronic hyperglycemia
accelerates the accumulation of advanced glycated end-
Diabetesmellitus(DM)isaprogressivechronicdiseasethat products (AGEs) (5), which results in local tissue alterations
hasahighlevelofmorbiditybecauseofthecomorbiditiesthat thatcanincreasesusceptibilitytoinfections(6).
occurduringdiseaseevolution,whichcancompromisepatient It isimportanttobeabletoidentifypatientswhohavean
qualityoflife(1).Oneofthemostimportantcomplicationsof elevated risk of developing oral complications related to
DMistheobservedincreaseinsusceptibilitytoinfections(2), invasivedentalprocedures.Thus,thisstudyaimedtoevaluate
likely due to impaired immunological defenses (3), which the frequency of clinical complications following invasive
havebeenassociatedwithincreasedconcentrationsofplasma dental procedures in type 2 diabetic patients based on their
levelsof glycemic control. Furthermore,this studysought to
determinethelevelsoffastingbloodglucose(FBG)andHbA1c
thatcouldbeconsideredsafetoavoidthesecomplications.
Copyright (cid:2) 2013CLINICS–ThisisanOpenAccessarticledistributedunder
thetermsoftheCreativeCommonsAttributionNon-CommercialLicense(http://
creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non- & SUBJECTS AND METHODS
commercial use, distribution, and reproduction in any medium, provided the
originalworkisproperlycited. Ethics statement
Nopotentialconflictofinterestwasreported. ThisstudywasapprovedbytheEthicsCommitteeofthe
DOI:10.6061/clinics/2013(03)RC01 Dentistry School of Ribeira˜o Preto, Sa˜o Paulo University,
427
Oralcomplicationsintype2diabetes CLINICS2013;68(3):427-430
MottaACetal.
Brazil (CAAE #0012.0.138.000-10). All subjects provided Dental School of Ribeira˜o Preto. Prior to performing any
writteninformedconsentpriortotheirparticipationinthis dental work, the levels of FBG, HbA1c, and fingerstick
study. capillary glycemia (FCG) were determined in all type 2
diabeticpatients.Sevendaysafterthedentalprocedure,the
Subjects frequency of clinical complications (surgery site infections
Type2diabeticpatientsandnon-diabeticpatientsover35 and systemic infections) in the three study groups was
years of age were selected and divided into three groups. analyzed. In addition, the presence of tissue necrosis,
The study cohort consisted of individuals of both genders purulent secretion, pain, edema, and dehiscence/wound
and a range of ethnicities. Group I consisted of type 2 breakdownwasexamined.Symptomswereregisteredusing
diabeticpatientswithadequateglycemiccontrol(FBGlevels a10-cmvisualanalogscale(VAS;0=nopainto10=extreme
below140mg/dlandHbA1clevelslessthan7%).GroupII pain). The correlations between clinical outcomes and
consisted of type 2 diabetic patients with inadequate dental procedures, clinical outcomes and symptoms,
glycemiccontrol(FBGlevels.140mg/dlandHbA1clevels and symptoms and type of dental procedure were also
.7%). Group III was the control group and consisted of evaluated.
non-diabetic patients (no symptoms of diabetes and FBG
levels ,100mg/dl). Diabetes diagnoses were made based Statistical analysis
on the World Health Organization (WHO) recommenda- Fisher’s exact tests were used to evaluate the differences
tions(7).Alldiabeticpatientsincludedinthisstudyhadmet inclinicaloutcomesafterinvasivedentalproceduresinthe
thediagnosticcriteriafordiabetesforatleastfiveyears.The three groups, the association between clinical outcome and
following inclusion criteria were used: at least six teeth, a proceduretype,andtheeffectsofgenderineachofthethree
requirement for dental surgery (simple extraction) or groups.TheseanalyseswereperformedusingSASsoftware
complex periodontal treatment (non-surgical scaling and (Statistical Analysis System - SASH 9.0 software; Cary, NC,
rootplanning).Theneedforextractionwasevaluatedusing USA). Differences in age, glycemic control, and symptoms
clinicalandradiographicexaminations.Therequirementfor reported by the patients between the three groups were
periodontaltreatmentwasevaluatedviaperiodontalscreen- analyzed using Kruskal-Wallis tests with Dunn post hoc
ingandrecording(PSR),andpatientsclassifiedasPSR3or tests, and these analyses were performed using R software
4 codes were selected. Subjects were excluded if they (R Foundation for Statistical Computing, Vienna, Austria;
presented with co-existing local or systemic infections, http://www.r-project.org). The data were reported as the
severe complications related to diabetes, or if they had means and standard deviation (SD), and the level of
received antimicrobial treatment for oral infections in the significance wassetat 5%for allanalyses.
previous threemonths.
& RESULTS
Study design
A case-control study was developed and performed The demographic characteristics and glycemic control of
between May 2010 and November 2011. The charts from the subjects are shown in Table 1. After reviewing 1,175
diabetic patients treated at the Diabetes Outpatient Clinics charts for inclusion and exclusion criteria, 147 type 2
oftheUniversityHospitaloftheMedicalSchoolofRibeira˜o diabetics were initially selected. However, only 28 subjects
Preto, Sa˜o Paulo University, were reviewed, and patients werefoundtobeeligibleforthecurrentstudy.Ofthese,13
that met the eligibility criteria were referred to the Dental subjectshadtype2diabeteswithadequateglycemiccontrol
School of Ribeira˜o Preto for dental treatments. Patients for (Group I), and 15 exhibited inadequate glycemic control
the control group were selected from the clinics of the (GroupII).Theother119patientswereexcludedforatleast
Table 1-Clinical characteristics of type2diabetic patients withadequate(Group I)and inadequate glycemic control
(GroupII)andnon-diabeticsubjects(GroupIII)andthefrequencyofsymptomlevels(0-5and6-10)reportedafterdental
invasive procedures.
Variables GroupI(n=13) GroupII(n=15) GroupIII(n=18) p-value
Gender*
Male 7(53.8%) 4(26.7%) 3(16.6%) 0.10{
Female 6(46.2%) 11(73.3%) 15(83.4%)
Age(years)
Mean¡SD 58.53¡6.11 52.86¡7.24 46.53¡7.61 ,0.01{
Capillaryglycemia(mg/dl)**
Mean¡SD 151.33¡39.80 240.93¡72.89 105.26¡22.91 ,0.01{
Fastingbloodglucose(mg/dL)**
Mean¡SD 134.76¡25.18 197.33¡71.79 88.73¡9.78 ,0.01{
HbA1c(%)**
Mean¡SD 6.5¡0.50 10.22¡1.33 - ,0.01{
Clinicaloutcomes*
No 12(92.3%) 13(86.6%) 17(94.4%) 0.81{
Yes 1(7.7%) 2(13.3%) 1(5.6%)
Symptoms(VAS)
0-5 12(92.3%) 14(93.4%) 17(94.4%) 0.80{
6-10 1(7.7%) 1(6.6%) 1(5.6%)
*Valuesshownasn(%);**valuesshownasthemeansandstandarddeviation(SD);{Fisher’sexacttest;{Kruskal-Wallistest;VAS:visualanalogscale.
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CLINICS2013;68(3):427-430 Oralcomplicationsintype2diabetes
MottaACetal.
oneofthefollowingreasons:FBGlevels.300mg/dland/ FCG=98mg/dl (Group III patient). Regarding the HbA1c
orHbA1clevels.10%,whichareassociatedwithcomplica- values, the three diabetic patients who had postoperative
tionsofdiabetes;nothavingatleastsixteeth;orrefusingto complications had HbA1c values as follows: 7% (Group I
participateinthestudy.Eighteennon-diabeticpatientswere patient)and9% and11%(Group IIpatients).
also studied as a control group (Group III). FBG, HbA1c, The use of antibiotics has been recommended for type 2
andFCGlevelswerehigherintype2diabeticpatientswith diabetics prior to dentoalveolar surgery (8,9) to prevent
inadequate glycemic control compared with those with surgical site infections and facilitate the healing process. In
adequateglycemic control. this study, antibiotics were not used prior to dental
The frequency of clinical complications was low and procedures in any of the groups, but the frequency of
similar(p=0.80)inthethreegroups,andthisfrequencywas clinical complications was low nonetheless. The similar
independentofglycemiccontrol(Table1).Ofthe46patients prevalence of surgical site infections in type 2 diabetic
examinedhere,onlyfour(8.6%)showedoralcomplications: patientswithadequateandinadequateglycemiccontroland
oneinGroupI,twoinGroupII,andoneinGroupIII.These innon-diabeticssuggeststhattherateofinfectionsmaynot
four patients were treated by dental extraction, and their depend on glycemic control, despite the reports of an
outcomes were all characterized by intra-oral swelling, increased risk of infections in diabetic patients (10). In
redness, pus, and wound dehiscence. All 27 patients addition, these results suggest that antibiotic prophylaxis
underwentscalingandrootplanning,whichdidnotinduce may only be appropriate in specific cases, not during
anycomplications.Thus,dentalextractionswereassociated routinepractice.Allofthepatientsinthecurrentstudywere
with increased numbers of complications compared with treated with local antibiotic irrigation, and the surgical
scaling androot planning(p=0.02) (Table2). wounds of all patients were clinically repaired within 10
Most patients (43/46; 93.4%) reported pain symptoms days.
ranging from 0 and 5 (VAS), but three patients reported The present study failed to identify a direct relationship
symptomsrangingfrom6to10(Table1).Allofthepatients between FBG levels or HbA1c values and postoperative
whoreceivedscalingandrootplanninghadVASscoresof5 complications; thus, it was impossible to suggest FBG or
or lower, and all three of the patients who reported HbA1c values that would be predictive of complications.
symptoms greater than 6 had undergone extractions (of 19 This study did reveal that dental extractions are more
total,15.7%)(Table2).However,nosignificantassociations frequently characterized by complications than scaling and
were observed between the clinical outcomes and symp- root planning procedures, but this effect was not linked to
toms(p=0.81)orbetweenthetypeofdentalprocedureand glycemiccontrol.Thelimitationsofthisstudyincludedthe
symptoms(p=0.20). small number of patients and the fact that postoperative
FBG values were not evaluated. It is possible that studies
& DISCUSSION with larger sample sizes might be sufficiently powered to
assess the impact of glycemic control on the occurrence of
This study evaluated the frequency of postoperative
postoperative complications.
dentalcomplicationsinpatientswithtype2diabetesbased
ontheirlevelsofglycemiccontrol.Theresultsdemonstrated & ACKNOWLEDGMENTS
a low frequency of complications, and no evidence of an
effectofglycemiccontrolonclinicaloutcomeswasobserved TheauthorsaregratefultoMsMilenaSaavedraLopesAmaralandMaria
(Table 1). Of the 46 patients who underwent invasive Aparecida Yoshiko Hirasawa Matuyama for assistance with sample
procedures, only four (8.6%) had surgical site infections, analysis.Dr.CristianeAparecidaNogueiraBataglionwassupportedbya
scholarship from the Coordination for the Improvement of Graduated
andthisoutcomeoccurredinpatientsfromeachofthethree
Personnel. The study was funded by the Foundation of Support to
groups:onepatientfromGroupI,twopatientsfromGroup
Teaching,ResearchandAssistanceofHCFMRP-USP(FAEPA).
IIandone patientfrom GroupIII.
ThefollowingFBGandFCGvalueswereobservedinthe & AUTHOR CONTRIBUTIONS
patients who had postoperative complications: FBG=
137mg/dl and FCG=225mg/dl (Group I patient); MottaACconceivedanddesignedthestudyanddraftedthemanuscript.
FBG=219mg/dl; FCG=300mg/dl and FBG=301mg/dl; Bataglion CA performed the study. Foss-Freitas MC, Foss MC, and
FCG=195mg/dl (Group II patients); and FBG=88mg/dl; KomesuMCparticipatedinthedesignandcoordinationofthisstudy.
& REFERENCES
Table2-Frequencyoftype2diabeticpatientspresenting
outcomes and symptoms basedonthe typeof dental 1. AmericanDiabetesAssociation.DiagnosisandClassificationofdiabetes
procedure. mellitus. Diabetes Care. 2011;34:S62-S69, http://dx.doi.org/10.2337/
dc11-S062.
2. FossNT,PolonDP,TakadaMH,Foss-FreitasMC,FossMC.Skinlesions
Procedure p-value** indiabeticpatients.RevSau´dePu´blica.2005;39(4):677-82,http://dx.doi.
org/10.1590/S0034-89102005000400024.
SRP Extraction
3. ShahBR,HuxJE.Quantifyingtheriskofinfectiousdiseasesforpeople
with diabetes. Diabetes care. 2003;26(2):510-3, http://dx.doi.org/10.
Outcomes*
2337/diacare.26.2.510.
No 27(100%) 15(78.9%) 0.02
4. Foss-FreitasMC,FossNT,DonadiEA,FossMC.InvitroTNF-aandIL-6
Yes 0(0%) 4(21.1%)
production by adherent peripheral blood mononuclear cells patients
Symptoms(VAS)* evaluated according to the metabolic control. Ann NY Acad Sci.
0-5 27(100%) 16(84.2%) 0.20 2006;1079:177-80,http://dx.doi.org/10.1196/annals.1375.027.
6-10 0(0%) 3(15.8%) 5. Vlassara H, Brownlee M, Manogue KR, Dinarello CA, Pasagian A.
Cachectin/TNFandIL-1inducedbyglucose-modifiedproteins:rolein
*Valuesshownasn(%);VAS:visualanalogscale;SRP:scalingandroot normaltissueremodeling.Science.1988;240(4858):1546-8,http://dx.doi.
planning;**Fisher’sexacttest. org/10.1126/science.3259727.
429
Oralcomplicationsintype2diabetes CLINICS2013;68(3):427-430
MottaACetal.
6. KomesuMC,TangaMB,ButtrosKR,NakaoC.Effectsofacutediabetes non-antimicrobialmechanisms.AdvDentRes.1998;12(2):12-26,http://
on rat cutaneous wound healing. Pathophysiology. 2004;11(2):63-7, dx.doi.org/10.1177/08959374980120010501.
http://dx.doi.org/10.1016/j.pathophys.2004.02.002. 9. TongDC,RothwellBR.Antibioticprophylaxisindentistry:areviewand
7. World Health Organization [Internet]. WHO/Diabetes; Disponible: practicerecommendations.JAmDentAssoc.2000;131(3):366-74.
http://www.who.int/topics/diabetes_mellitus/en/. 10. RaoDD,DesaiA,KulkarniRD,GopalkrishnanK,RaoCB.Comparison
8. Golub LM, Lee HM, Ryan ME, Giannobile WV, Payne J, Sorsa ofmaxillofacialspaceinfectionindiabeticandnondiabeticpatients.Oral
T. Tetracyclines inhibit connective tissue breakdown by multiple SurgOralMedOralPatholOralRadiolEndod.2010;110(4):e7-12.
430
