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S C I E N T I F I C A R T I C L E

The healing of dental extraction sockets in patients withType 2 diabetes on oral hypoglycaemics: a prospectivecohort

S Huang,* H Dang,* W Huynh,* PJ Sambrook,* AN Goss*

*Oral and Maxillofacial Unit, Royal Adelaide Hospital, South Australia.School of Dentistry, The University of Adelaide, South Australia.

ABSTRACTBackground: The aim of this study was to determine whether there is a difference in delayed healing following dentalextractions for Type 2 diabetics on oral hypoglycaemics and non-diabetic patients.Methods: Prospective patients referred for dental extractions were recruited into two groups: known diabetics and non-diabetics with no conditions associated with poor healing. All had a random blood glucose level (BGL). Extractions wereperformed using local anaesthesia. Delayed healing cases were identified and statistical evaluation performed to identifyrisk factors.Results: There were 224 Type 2 diabetics on oral hypoglycaemics (BGL 7.51, range 4.117.4) and 232 non-diabetics.The diabetic group were older, more males and less smokers than the control group. Twenty-eight patients, 12 (5%) dia-betic and 16 (7%) control group, had socket healing delayed for more than one week but all healed in four weeks. Therewere no statistical differences between delayed healing and age, gender, diabetic state, BGL or smoking. The youngercontrol group had more healing problems.Conclusions: The traditional view that diabetics have increased delayed healing was not supported. Type 2 diabetics onoral hypoglycaemics should be treated the same as non-diabetic patients for extractions.

Keywords: Diabetes, Type 2, blood glucose levels, extractions, delayed healing, prospective cohort controlled study.

Abbreviations and acronyms:BGL = blood glucose level; IFG = impaired fasting glucose; IGT = impaired glucose tolerance; OMS =oral and maxillofacial surgery.

(Accepted for publication 16 July 2012.)

INTRODUCTION

Traditionally in dentistry diabetics are considered tohave increased healing problems related to dentalextractions, periodontal surgery and wearing ill-fitting

dentures.1

They are also considered more likely tohave infections. Although this may be so for poorlycontrolled Type 1 diabetics, there is only anecdotalsupport for this view for Type 2 diabetics on oralhypoglycaemics. There are no evidence based studiessuch as case controlled cohort studies for dental sur-gery in Type 2 diabetes.

This is an important evidence based deficiency asType 2 diabetics constitute 90% of all diabeticpatients. Recently after the completion of the datacollection of the present study, a report comparingwell controlled with poorly controlled diabetics, asmeasured by blood glucose level (BGL), haemoglobin

Alc (HbAlc) and endorganic scores was published. Itfound no difference in healing.2

Diabetes is a common metabolic disorder character-ized by an inability to regulate blood glucose due toinsulin deficiency or resistance. Type 1 diabetes (previ-

ously known as insulin-dependent, juvenile or child-hood-onset) is characterized by deficient insulinproduction whereas Type 2 diabetes (formerly callednon-insulin-dependent or adult-onset) results from rel-ative insulin deficiency and tissue insulin resistancecausing abnormal BGLs despite secondary hyperinsuli-naemia.3,4 In the AusDiab Study of 2002 it was foundthat 7.4% of Australian adults were diabetic and afurther 16.4% were prediabetic.5 For every twoknown diabetics it has been found that there is atleast one unknown diabetic. This number is increasedby the two prediabetic states of impaired fasting glu-cose (IFG) and impaired glucose tolerance (IGT).

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Patients with prediabetes do not meet the criteria forbeing diagnosed with diabetes but have glucose levelshigher than those considered normal.6 For IFG, it is afasting BGL of 6.17 mmol/L and for IGT, it is anon-fasting BGL of 7.811.0 mmol/L. Each year,310% of people with prediabetes will go on to

develop diabetes.4 The clinically relevant BGLs are7.8 mmol/L for prediabetes and 11.0 mmol/L for dia-betes.7 Another useful measure of long-term glycaemiccontrol is the haemoglobin Alc (HbAlc) test where thetarget is 6.57.0%, with above 8.0% being an indica-tor of poorer control. It is recommended that dentistsdetermine the stability of known diabetics by meansof the BGL and HbAlc, either by patient history,advice from their medical practitioner or by directlyperforming the tests prior to commencing surgery.7

Poor glycaemic control predisposes to developmentof a range of complications that have been broadly

categorized as macrovascular, microvascular and neu-ropathic.8 Microcirculatory deficiencies, in particular,can have significant bearing on wound healing follow-ing surgical procedures. An intact microcirculation isrequired for tissue nutrition, removal of waste prod-ucts, inflammatory responses and temperature regula-tion.9 In diabetics, changes to the capillaries such asthickening of the basement membrane result in alteredpermeability, impeded migration of leucocytes andimpaired hyperaemia, causing underperfusion duringtissue stress and tissue hypoxia.9,10 These changes canadversely affect the outcome of surgery, resulting inpoor wound healing and wound infection.11,12 This

has been most clearly documented in relation to car-diothoracic procedures where poorly controlled dia-betic patients undergoing coronary bypass surgeriesexperienced increased morbidity and mortality,13

increased rates of postsurgical infections14 and worsehospital outcomes.15,16 Conversely, maintenance oftight perioperative glycaemic control for coronarybypass patients has been shown to significantlydecrease infections and other adverse outcomes.17 Ithas been shown that diabetic complications can occurduring prediabetes, particularly microangiopathy suchas diabetic retinopathy.18 It is for these reasons that

known diabetics are offered counselling on nutritionand lifestyle including smoking cessation.5

In dentoalveolar surgery, diabetic patients could beexpected to suffer similar complications to thoseobserved in other surgical procedures. However, theoral environment with the forces of mastication, highbone turnover, high vascularity, saliva and the con-stant reservoir of microorganisms is distinct fromother parts of the body, thereby making generaliza-tions from other surgical sites limited.19

There have been a limited number of studies usingexperimentally induced diabetes in rats. These animalshave an uncontrolled insulin dependent diabetic state

and not surprisingly dental extraction wounds healpoorly, often with alveolar destruction.20 However,this does not represent a current clinical situation inan advanced country such as Australia unless both thepatient and their treating dentist completely misman-age an unstable Type 1 diabetic state. This may occa-

sionally occur and the patient ends up in hospital,requiring specialist management. Such cases are notreported but the two consultant oral and maxillofacialsurgeons (ANG, PJS) in this study have encounteredsuch cases.

The aim of this study is to investigate and comparethe difference in healing between Type 2 diabetics andnon-diabetics, and whether differences in a randomBGL are of any significance.

METHODS

This prospective study was performed in the exodon-tia clinic of the oral and maxillofacial surgery (OMS)unit in the outpatient clinic at the Adelaide DentalHospital, South Australia. Appropriate ethics approvalfrom the Royal Adelaide Hospital was obtained(RAH REC 091115).

Patients 18 years and over who were referred forextractions under local anaesthesia during the aca-demic year 2010 and had a detailed medical historywere approached to give written consent to beinvolved in the study. Exclusion criteria related toknown conditions which may impair healing ofextraction namely: Type 1 diabetes and insulin depen-

dent Type 2 diabetes; HIV/AIDS; chemotherapy; sys-temic steroids; irradiation to the head and neck;dental infections with systemic involvement; bis-phosphonates; anticoagulant and antiplatelet treat-ment; and major benign or malignant pathologywithin the jaws. Patients unable to give consentthrough physical or mental disability were alsoexcluded.

All patients had a random BGL taken after adminis-tration of the local anaesthetic (2% lignocaine with 1in 80 000 adrenaline) using a glucometer (OptimumXceed Abbott Diabetes Care, Doncaster, VIC, Aus-

tralia). Patients were initially assigned to two groups:known Type 2 non-insulin dependent diabetics onoral hypoglycaemics and the control group withoutconditions known to impair healing.

The intra-alveolar extraction of erupted teeth wasthen performed with forceps and elevators by finalyear dental students under the supervision of OMSstaff. Antibiotics were only prescribed if there wasclear evidence of localized acute odontogenic infectionwith pus present. Patients with spreading infectionwere excluded. Patients were offered follow-up reviewat one week or if they declined, advised to contact orreturn to the OMS clinic if they had problems.

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The random BGLs of the control group werechecked. Those with a BGL above 7.8 mmol/L werecounselled by OMS staff and referred in writing totheir general medical clinic.4,7 Diabetic patients witha BGL above 11 mmol/L were also advised and coun-selled.7

The results of completed questionnaires wereentered into a Microsoft spreadsheet on a standalonePC at the end of each day. The patient records werereviewed at four weeks by one researcher (SH) todetermine who had returned or reported delayed heal-ing. This included dry socket, bony sequestra orexcess granulation tissue after one week.

The patients medical practitioner was contacted ateight weeks to determine the outcome of investiga-tions for those non-diabetic patients with a BGLabove 7.8 mmol/L. Patients who demonstrated to bediabetic were reassigned to the diabetic group.

Data were analysed using SAS software Version9.3 (SAS Institute Inc, Cary, NC, USA). The odds ofdelayed healing were compared between the diabeticsand non-diabetic groups using logistic regression, withresults expressed as odds ratios with 95% confidenceintervals. Logistic regression was also used to test theassociation between perioperative BGL and the oddsof delayed healing. Lastly, a multivariate logisticregression model was used to test whether age, genderand smoking had any effect on delayed healing.Throughout all analyses a two-tailed p-value of 0.05was used to indicate statistical significance.

RESULTS

Five hundred and ten patients who met the inclusioncriteria for the study were approached to participate.Thirty (6.0%) declined to give consent, all were non-diabetics and received routine extractions outside ofthe trial. Of the remaining 480, 222 were knownType 2 diabetics on oral hypoglycaemics and not tak-ing insulin, with an average BGL of 7.5 mmol/L,range 4.1 to 17.4. Two hundred and fifty-eight werein the control group but of these, 32 had a randomBGL of above 7.8 mmol/L. All of these were advised

to seek medical advice and were given a written refer-ral with a copy directly to the medical clinic. Onewas found to be a diabetic, one a prediabetic and

these were reassigned to the diabetic group, making atotal of 224 in the diabetic group. Six were found notto be diabetic or prediabetic and remained in the con-trol group, making a total of 232.

Twenty-four patients, despite verbal and writtenadvice, did not seek medical attention. Of these, six

made appointments but did not attend. One hadsevere mental issues and was admitted to an appropri-ate facility and found not to be diabetic. Seventeenwere not known to the medical clinic they nominatedand had not been seen. These 24 patients wereexcluded from the trial.

Twenty-eight patients had healing delayed beyondone week; 12 (5%) in the diabetic group and 16 (7%)in the non-diabetic control group. All had fully healedwithin four weeks. There were no cases of osteomyeli-tis or osteonecrosis of the jaws.

The age, gender, BGL, smoking status and adverse

outcomes are presented in Table 1. The diabeticgroup was on average 17 years older with more malesand less smokers. They had less delayed healingevents. The relationship of the delayed healing toBGL is presented in Table 2. The relationship of thedelayed healing to smokers is presented in Table 3.

Evaluation of the association between diabetic sta-tus and adverse outcomes showed that while the oddswere 30.9% higher in the non-diabetic group, 16(7%) vs 12 (5%), the difference between groups wasnot statistically significant (p = 0.49). In terms of theassociation between BGL and adverse outcomes, forevery unit increase in BGL the odds of adverse out-

comes increased by 0.9%, though this was also notstatistically significant (p < 0.93). An assessment ofother factors showed that there was no difference inthe odds of adverse outcomes according to age(p = 0.78), gender (p = 0.98) and smoking (p = 0.24)status.

DISCUSSION

This study shows that there was no statistically signifi-cant difference in post-extraction outcome betweenType 2 diabetics on oral hypoglycaemics and the con-

trol group. The number of previously unrecognizeddiabetics found in this study was low. Only 2 (25%)of the 8 patients with elevated BGL, whose outcome

Table 1. Demographics and overall outcome

Group n Age Gender BGL AbnormalBGL

Smoker Delayedhealing

Mean Range n % Mean Range n % n % n %

Non-diabetics 232 46.8 1688 M 105 45 5.2 1.99.2 2 0.86 90 38.8 16 6.9F 127 55

Diabetics 224 63.9 1987 M 141 63 7.5 4.117.4 86 38.4 43 19.2 12 5.4F 83 37

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was known, were subsequently proven to have diabe-

tes or prediabetes. The 24 with elevated BGL who didnot attend medical follow-up had an unknown status.The AusDiab study in 2002 found an incidence of3.7% unknown diabetics and 16.4% with prediabetes,or 20%, in an adult Australian population.5 The Aus-Diab study was very large and is thus difficult todirectly compare to this relatively small sample. How-ever, the numbers are of similar order.

The study population is different to the usual gen-eral dental population in that all the patients werereferred to the exodontia clinic of a specialist OMSunit. The referral base is from the community dentalservice, the public outpatient clinics of the Royal

Adelaide Hospital and other major teaching hospitals.As such all the patients have disability or other gov-ernment health care cards. Previous audits have shownthat as well as difficult extractions, over two-thirdsare significantly medically compromised. However,the initial assessment and extractions are performedby final year dental students with close supervision byOMS staff. Only 2 of the 480 patients, 1 from eachgroup, required formal surgical extractions. In thenon-diabetic control group, 3 had acute oro-antralfistulae created from maxillary extractions and allwere immediately closed by the OMS staff without

sequelae.Besides their medical complexity, frequently includ-

ing mental health issues, many were patients whosought only extractions for dental treatment. Mostwere not interested in attending follow-up appoint-ments citing transport, parking, travelling and waitingtime issues as reasons. Thus some patients who ini-tially had difficulty may have attended their localcommunity clinic or general medical practitioners.However, if there were ongoing issues the patientwould have been referred back. There are no otherpublic OMS services available to them. These patientattitudes to their overall health were reflected in the

24 of 32 with abnormally high BGLs who did notseek follow-up from their general medical practitionerdespite being encouraged to do so. Therefore, thisstudy group represents a more challenging populationthan those commonly seen in a private general prac-tice by general dentist.

The original plan for the study was that the diabeticand non-diabetic groups would be of similar age andgender, but this did not eventuate. The diabetic groupwas older on average by 17 years and there weremore males. Increased age and male gender are riskfactors for delayed healing.21 Conversely, more of thecontrol group were smokers, also an important factorin delayed healing.21 Although there were no statisti-cal differences, the clinical impression was that thediabetic group had less delayed healing than the youn-ger, more female control group.

Overall, the study population had 29.2% smokers,

which is higher than the recently reported figure of19% for the adult Australian population.22 This proba-bly relates to the lower socio-economic status of thestudy population. However, there was an importantdifference between the non-diabetic group of whom39% smoked and the diabetic group with only 19% ofsmokers. This reflects the effort put in by diabetic edu-cators as smoking and diabetes result in a high risk ofcardiovascular and peripheral vascular disease.5

At the time of development and implementation ofthis study there were no prospective cohort studies onthe effect of diabetes on extraction wound healing.Recently, a broadly similar study has been published

which compared the relationship of glycaemic controlbetween well and poorly controlled diabetics.2 Theyfound no statistically significant difference betweenthe two groups. This is a similar outcome to the pres-ent study. However, on detailed analysis there aresome methodological issues with the study by Arono-vich et al.2 They combined both Type 1 and Type 2diabetics and did not have a non-diabetic controlgroup. Thus, the present study looks at a homogenousgroup of Type 2 diabetics on oral hypoglycaemics andcompares them to a non-diabetic population treatedby the same staff, in the same clinic over the same

time period. This strengthens the specific value of thestudy to dental practice.

It is concluded that there is similar healing betweenType 2 diabetics on oral hypoglycaemics and non-diabetic patients. Special precautions including warn-ings about adverse healing and prophylactic antibioticsfor routine extractions are not required.

ACKNOWLEDGEMENTS

We acknowledge the participation of the final yearBDS class of 2010, The University of Adelaide forthis study. The support of the OMS clinic staff,

Table 2. Relationship between delayed healing andBGL

BGL Diabetic Non-diabetic

Below 7.8 7 (5.1%) 16 (7.0%)7.811 5 (6.3%) 0 (0%)Above 11 0 (0%) 0 (0%)

Table 3. Relationship between delayed healing andsmokers

Smokers Diabetic Non-diabetic

Yes 1 (2.3%) 4 (4.4%)No 11 (6.1%) 12 (8.5%)

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particularly the registered nurses, is acknowledged.The statistical advice of Dr T Sullivan of the DataManagement and Analysis Centre at the University ofAdelaide is gratefully acknowledged.

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Address for correspondence:Professor Alastair N Goss

School of DentistryThe University of Adelaide

Adelaide SA 5005Email: alastair.goss@adelaide.edu.au

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