RAPID 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. 428 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. 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