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microorganism. It is not only the host defense thatdetermines the outcome of infection, but the timing andappropriateness of antimicrobial treatment as well.

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1

aPoCotakbAsS.DKacPrS.DInddPrMapitaeDiHoRe201107 2doiDiabetes is a metabolic syndrome characterized byppropriate elevation of plasma glucose level associ-d with changes in the lipid, protein, and carbohy-te metabolism for which a relative or absolute lackinsulin is responsible. Associated degenerative com-

hyperglycemia.In addition to impaired host defence mechanism,

other factors may also increase the susceptibility ofdiabetic patients to infection. Microangiopathy impairsleukocyte migration by thickening the capillary base-ment membrane and macroangiopathy favors acral skinand soft tissue infection.

Some reports give Streptococcus as the major caus-ative organism for infection, whereas a few have Kleb-siella pneumoniae as the predominate causative organ-ism. In odontogenic infections it has been documentedthat the organisms that affect diabetic individuals mightbe different from those in individuals who are notdiabetic.2

One unanswered question is whether the increasedrisk in diabetic individuals is attributable to hypergly-cemia itself or other associated features found in dia-betic patients. The severity of infection, hospital stay,and complications associated with the infection areconsidered to be greater in diabetic individuals.3

stgraduate, Department of Oral and Maxillofacial Surgery, S.D.Mllege of Dental Sciences and Hospital, Sattur, Dharwad, Karna-a, India.sociate Professor, Department of Oral and Maxillofacial Surgery,.M College of Dental Sciences and Hospital, Sattur, Dharwad,

rnataka, ndia.ofessor and Head of the Department, Department of Microbiology,.M. Medical College and Hospital, Sattur, Dharwad, Karnataka,ia.ofessor and Head of the Department, Department of Oral &xillofacial Surgery, S.D.M College of Dental Sciences and Hos-l, Sattur, Dharwad, Karnataka, India.rector, Craniofacial Unit, S.D.M College of Dental Sciences andspital, Sattur, Dharwad, Karnataka, ndia.ceived for publication Jan 31, 2010; returned for revision Mar 15,0; accepted for publication Apr 8, 2010.9-2104/$ - see front matteromparison of maxillofacial space infenondiabetic patientsDipesh D. Rao, MDS,a Anilkumar Desai, MDS,K. Gopalkrishnan, MDS, FDSRCS,d and C. BhaS.D.M COLLEGE OF DENTAL SCIENCES AND HOSPIT

roduction. Orofacial space infections are common prese. One of the main factors determining the spread of infest common systemic illness suppressing the immunity ofections. This study was carried out to compare the spaceefficacy of empirical antibiotics, the length of hospital s

maxillofacial space infection of odontogenic origin in dithodology. A 4-year prospective study was carried out oontogenic origin. The patients were divided into 2 groupsults. A total of 111 patients were identified out of whiceptococcus species with submandibular space being thepirical antibiotic used was amoxicillin plus clavulanic anclusion. Streptococcus species is still the most commonpatient. The same empirical antibiotic therapy of amoxi

th hyperglycemia control and surgical drainage of infectitients as well. (Oral Surg Oral Med Oral Pathol Oral Ra

sk of infection depends on several factors, includingst defence mechanisms, functional or anatomical ab-rmalities of the host, and virulence of the infectingsig010 Mosby, Inc. All rights reserved.

:10.1016/j.tripleo.2010.04.016n in diabetic and

. Kulkarni, MD,cao, MDS, FDSRCPS,e Karnataka, India

ns in maxillofacial clinics even in the post-antibiotics the host defense mechanism. Diabetes is one of thedividual and increasing their susceptibility tolved, the severity of infection, the virulent organism,d the complications encountered in the managementpatients as compared with nondiabetic patients.ients with maxillofacial space infection ofe basis of presence or absence of diabetes.ere diabetic. The organisms commonly isolated were

common space involved in both the groups. Thembined with metrogyl in 70.27% cases.ative pathogen irrespective of the diabetic status ofplus clavulanic acid combined with metrogyl alonglded satisfactory resolution of infection in the diabeticdod 2010;110:e7-e12)

cations include macroangiopathy, microangiopathy,d neuropathy. The prevalence of diabetes is increas-

worldwide with diabetic individuals usually havingIn view of the preceding scenario, a study was de-ned with an objective to comprehend the severity of

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OOOOEe8 Rao et al. October 2010ection, nature of microorganisms, antibiotic sensitiv-of the microorganisms, and the length of hospital

y in diabetic individuals and to compare it withndiabetic individuals.

TIENTS AND METHODSA prospective study was carried out for 4 years ontients who reported with maxillofacial space infec-n of odontogenic origin in our hospital. A total of1 patients who needed hospitalization for surgicalinage of the infection were included in the study andided into 2 groups:

Group I: Thirty-one patients who had a fastingblood glucose level more than 130 mg/dL (7.2mmol/L) or had a known history of diabetes but hadcontrolled sugar levels were also included in thediabetic group.Group II: Eighty patients were included in the non-diabetic group who presented with maxillofacial spaceinfection and had normal blood glucose levels at thetime of reporting, no history of diabetes, and their sugarlevels always remained within normal limits duringhospital stay without hypoglycemic agents.

The patients who were not included in the study were

Patients with head and neck space infection of non-odontogenic origin.Patients who did not require hospitalization and sur-gical drainage of the infection.Patients with unknown antibiotic intake beforereporting.

Written consent was obtained from all the patientsd the study received ethical clearance from the insti-ions ethical board.Pus samples from the site of infection were collectedthe operating table under general anesthesia whileining the infection. The samples were collected on 2ferent swabs: one swab was used for culture whereas

ble I. Comparison of spaces involved in diabetic andpace involved Diabetic (31 pts) % Nmandibular 12 38.71

ccal 9 29.03dwigs angina 7 22.58masseteric 7 22.58mental 6 19.35poral 5 16.13

nine 3 9.68rygomandibular 3 9.68eral pterygoid 1 3.23diastinitis 1 3.23lingual 0 0.00

, patients.other was used for Gram staining. The specimens then immediately sent for microbiological investi-tion. The sample was inoculated on blood agar andacConkeys agar and incubated at 37C for 24 hours.e growth was identified by standard techniques.The antibiotic sensitivity testing was done by Kirbyuer disk diffusion method. The susceptibility testsre performed as per Clinical Laboratories Standardtitution (CLSI) guidelines. The results were reportedsensitive, moderately sensitive, or resistant to theferent antibiotics.The diabetic and nondiabetic groups were comparedthe following parameters:

The spaces involved (on clinical examination)FeverThe white blood cell (WBC) countThe organisms isolated from the cultureThe sensitivity of the organismsNeed to change the empirical antibioticThe duration of hospital stay

The results obtained were subjected to unpaired t testd chi square test comparisons.

SULTSThe age group of diabetic individuals was (mean ) 47.97 10.11years and of the nondiabetic indi-uals was 43.70 14.64 years.

The space most commonly involved in both thebetic and nondiabetic individuals was the subman-ular space, followed by the buccal space and sub-sseteric space (Table I). Patients presented withdwigs angina in 22.58% of diabetic and in 16.25%nondiabetic patients. The diagnosis of the involved

aces was always confirmed intraoperatively.On presentation, the axillary body temperature wasasured and 64.52% of diabetic patients were febrilepresentation whereas only 37.50% of nondiabetic

abetic patientstic (80 pts) % Total (111pts) %49 61.25 61 54.9530 37.50 39 35.1413 16.25 20 18.0120 25.00 27 24.3215 18.75 21 18.928 10.00 13 11.716 7.50 9 8.11

12 15.00 15 13.515 6.25 6 5.410 0.00 1 0.903 3.75 3 2.70SDvid

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OOOOEVolume 110, Number 4 Rao et al. e9ividuals had raised temperatures, which is statisti-lly significant (P .01).The WBC count of both the diabetic and the nondi-etic groups was more than 12,000 cells/mm3 with nonificant difference (P .67).All the patients were started on intravenous antimi-bial therapy immediately on presentation. The dia-

tic patients received insulin therapy, which was ti-ted by the physician on their basis of their dailyod glucose levels.

Seventy-eight patients of the 111 cases were startedamoxicillin plus clavulanic acid combination andtrogyl as the empirical antibiotic. Only 3 of 31betic patients and 8 of 80 nondiabetic patients wereistant to amoxicillin of which 1 diabetic patient andondiabetic patients were found to be resistant to thevulanic acid combination as well.Overall there was need to change the antibiotics inly 12.61% of total cases.In the samples collected, the sterile swab for cultured bacterial growth in 56 patients of which 15 werebetic and 46 were nondiabetic patients. The Gramining was positive in an additional 6 diabetic and 15ndiabetic patients. There was polymicrobial growth4 and 3, diabetic and nondiabetic individuals, respec-ely.Of the organisms isolated, Streptococcus spp. was thest common bacteria in both the diabetic (16.13%) andnondiabetic groups (26.25%). Klebsiella pneumoniae

s the second most common organism in diabetic pa-nts, present in 12.9% of patients (Table II).The diabetic patients were found to have a compar-vely longer hospital stay than the nondiabetic pa-nts with the mean number of days being (mean ) 9.51 8.16 days and 6.15 3.64 days, respec-ely (P .003)

SCUSSIONThe treatment of orofacial infections is part of aneryday practice in oral and maxillofacial surgery.

ble II. Organisms isolated from diabetic and nondiabeOrganism isolated Diabetic (31 pts) %

terococcus 2 6.66herischia coli 0 0.00

sobacterium 0 0.00bsiella pneumoniae 4 12.90eptococcus spp. 5 16.13phylococcus aureus 2 6.45udomonas 2 6.45growth/Gram positive 11/5 51.61cobacterium 1 3.23inomycetes spp. 0 0.00

, patients.ontogenic abscess-forming infection usually spreadso the potential anatomical spaces present in the orald maxillofacial region. The area of least resistanceually governs the spread with the host defense mech-ism and virulence of the organism playing an impor-t role as well.4The poor host response is multifactorial and diabetess long been considered as one of the factors reducingst response. One of the serious complications ofbetes includes predisposition to infections. Diabeticividuals are not only at high risk for infectiousease but it is also believed that they often respondorly to infections once they occur.5The mechanisms in which diabetes predisposes toection may be attributable to hyperglycemia, dis-bed neutrophil bactericidal function, cellular immu-y, and complement activation. The mentioned de-ts of the immune system along with the vascular

normalities present in diabetic patients render them ather risk for a variety of invasive infections such as

ogenic bacterial infections, necrotizing infections,d fungal infections.Many authors have carried out the comparison ofection type and treatment outcome between diabeticd nondiabetic patients. A sundry of results have beentained. In a study that compared the deep neck spaceections in diabetic and nondiabetic patients, the au-rs concluded that patients with diabetes mellitusre more susceptible to deep neck infection.6 How-er, the association between maxillofacial space infec-ns of odontogenic origin and diabetes mellitus hasen rarely mentioned.The most commonly involved space in both thebetic and nondiabetic patients in this study was the

bmandibular space, followed by the buccal space andbmasseteric space. In a few studies, the parapharyn-al space was the most commonly involved space inbetic patients,7,8 whereas the submandibular spacethe buccal space was found to be more involved inndiabetic individuals.8,9

tientsabetic (80 pts) % Total (111 pts) %

5 6.25 8 7.212 2.50 2 1.801 1.25 1 0.903 3.75 5 4.50

21 26.25 26 23.420 0.00 2 1.803 3.75 5 4.50

19/15 42.50 50 45.051 1.25 2 1.801 1.25 1 0.90we

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OOOOEe10 Rao et al. October 2010Ludwigs angina is one of the most common presen-ions in patients with diabetes in a substantial numberthe reported studies.6,7 In this study, 7 (22.58%)betic and 13 (16.25 %) nondiabetic patients reportedth Ludwigs angina. The difference between the 2ups was statistically insignificant. This low signifi-

nce can be attributed to the poor socioeconomicckground of the patients, where the host defensesght be altered in nondiabetic individuals as well.Pyrexia occurs owing to the hypothalamicthermo-ulation centers response to chemicals induced by

cterial cell components such as endotoxins or cellll fragments. On presentation, the patients in thebetic group were found to be more febrile than thosethout diabetes. This result indicates that the patientso have diabetes and suffer from infection may haveher penchant toward bacteremia. The result is in

ison with other studies, which show a significanttistical correlation between raised body temperaturesing to decreased host response in diabetic patients.10The cellular, biochemical, or molecular basis of thecline in host defenses leading to increased infectionsdiabetic patients is yet to be conclusively established.BCs and especially the neutrophilic polymorphonuclearkocytes (PMNs) play an essential role in resistanceard infectious agents. Reduced PMN function is asso-

ted with increased bacterial susceptibility, especially inbetic individuals.11Acute bacterial infections trigger neutrophil releasem the bone marrow and thus an increase in these

lls in the peripheral blood is a useful indicator ofection. In this study as well, the WBC count in bothdiabetic and nondiabetic groups was raised above

,000 cells/mm3 and infection per se can thus be heldponsible for increased WBC levels irrespective ofunderlying coexisting diabetic status. Perhaps WBC

unt is more useful in assessing the improvement orression of a patients response to therapy, rather thandicting the actual patient status.12

The patients requiring hospital admission and surgi-l drainage received preoperative intravenous empiri-l antibiotics and this was followed postoperativelyth intravenous and oral antibiotics based on the cul-al and sensitivity reports. A combination of amoxi-lin plus clavulanic acid and metrogyl was used in% of cases; 64.52% in diabetic and 72.50% in non-betic patients. The next commonly used empirical

tibiotic regime was the combination of cefaperazonelbactum and metrogyl in 7.50% of nondiabetic indi-uals and, along with gentamycin, it was used in8% of diabetic individuals. This change in empirical

tibiotic was done because of the patients previoustory of antibiotic administration. Use of beta-lactamempirical antibiotics in spite of the apparent rise ofvitro resistance, infections are still responding.wever, addition of metronidazole into the regimen

s also been preferred.13 Studies conducted to identifyempirical antimicrobial therapy for odontogenic

ections have stated the use of amoxicillin with met-idazole as one of the most effective regimens.14-16

ttumarthy et al.17 studied the sensitivity of Strepto-ccus species to antimicrobials and found that amoxi-lin/clavulanate exhibited good potency. The admin-ration of amoxicillin with clavulanic acid aspirical antibiotic in our cases has proven effective inresolution of infection and only 3 of 31 diabetic andf 80 nondiabetic patients were found to be resistantamoxicillin. This suggests that presently there is noed to subject the patients to another antibiotic regi-n. The combination of amoxicillin and clavulanic

id along with metrogyl can work effectively in bothdiabetic and nondiabetic patients.

Organisms commonly isolated from odontogenicace infections include the Streptococcus species inst studies.9,18,19 Klebsiella pneumoniae has beenlated as the predominant infectious organismdiabetic patients.2,7In the present study, Streptococcus species wasnd to be the most common organism isolated in

.13% of diabetic and 26.25% nondiabetic patients.e second most common organism isolated in thebetic group was Klebsiella pneumoniae in 12.90%

tients.There was a high occurrence of no growth in ourlture reports. A total of 45% of cases yielded nowth but on direct smear examination, Gram stain

owed the presence of organisms in 40% of thoseses. The presence of organisms on Gram stain andlure to grow on aerobic cultures is a common find-. This may be attributable to anaerobic infections,

llection of sample after antibiotic dose, and occasion-y loss of organisms during handling, transportation,d processing of the samples.Polymicrobial infections were present in 4 diabeticd 3 nondiabetic patients.The failure to isolate anaerobic organisms had noect on the treatment outcome, as most of the patientsd good resolution of the infection. Consequently, thee of the same empirical antibiotic (amoxicillin/cla-lanic acid metrogyl) in both aerobic and anaerobicanism infection cannot be overlooked.

The complications encountered in both groups in-ded the need for reexploration and respiratory dis-ss. Deep neck space infections are difficult to iden-y and have been reported more frequently in diabetictients.2,6In this study there was a need for reexploration in 6ses, 3 each in the diabetic and the nondiabetic groups.

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OOOOEVolume 110, Number 4 Rao et al. e11e major complications were descending mediastini-, carotid space abscess, and residual lateral pharyn-al space infection in the nondiabetic group. In thebetic group a case of descending mediastinitis oc-

rred after surgical drainage of the primary spaceection. Death occurred in 1 patient owing to diabetictoacidosis, which ensued even after starting the pa-nt on careful hypoglycemic measures. None of ourtients underwent tracheostomy for airway manage-nt as reported in other studies.2The outcome of most of the infections with similarsentation was the same when the diabetes wasught under control using insulin therapy titrated as

r the physicians advice. This is similar to a studyt compared the outcomes of patients with infection

ving controlled diabetic and nondiabetic individuals;authors found that in spite of the higher incidence oftic shock in patients with diabetes the response to

atment after glycemia control in both patient groupss similar.7,20 Therefore, consultation with a diabe-ogist is recommended to control random blood sugarels to less than 130 mg/dL.The severity of the infection usually depends on thember of spaces involved, site of the space involved,toxic state of the patient, general health condition ofpatient, associated systemic illness, and the timingpresentation. The patient with greater severity ofection needs to stay in the hospital longer until thereimprovement in the toxic state of the patient and theection has subsided.In this study, when the hospital stay was comparedtween diabetic and nondiabetic patients it was foundt there was a highly significant difference. The dia-

tic patients had stay duration of (mean SD) 9.516 days, whereas that of the nondiabetic individualss 6.15 3.64 days (P .0033). The high differencehospital stay in spite of similar outcome to surgicalinage and response to antibiotics of both the groups

n be attributed mainly to the protocol of correctingblood glucose levels of diabetic patients before

charge.Rapid resolution of the infection and dramatic im-vement in the patients general status has been noteden simple basic fundamentals of intravenous antibi-cs and drainage of the infection are performed.21 Its also been reported that improved management ofbetic individuals will lead to better prognosis with-t any difference between the diabetic and nondiabetictients with similar severity of infection.22Thus, this study gives insight into the managementtocol to be used for patients with diabetes. The

tients, irrespective of the diabetic status, usually re-ond well to the basic treatment principles for spaceections with empirical antibiotics along with glyce-a control.

NCLUSIONThe corner stone of management of space infectionthe oral and maxillofacial region remains the same inbetic and nondiabetic patients.The results obtained from our study lead to thelowing conclusions:

Diabetic patients have a higher penchant towardbacteremia that can be determined because morepatients were febrile at presentation (64.52%).

The commonly involved space in both the diabeticand the nondiabetic patients was the submandibularspace, 38.71% and 61.25% patients respectively,whereas Ludwigs angina was present in 22.50%and 16.25% patients, respectively.The response to empirical antibiotic therapy ofamoxicillin/clavulanic acid metrogyl along withsurgical drainage of the infection under general an-esthesia provides satisfactory outcome when thediabetic patients have controlled glucose levels. Hy-perglycemia can be thus considered as the majorcontributing factor for the altered host response indiabetic patients.The organisms commonly isolated in both thegroups are Streptococcus species and antibiotics thataddress these organisms should be used as the firstline of drugs. This can avoid unnecessary use ofbroad-spectrum antibiotics and reduce antibiotic re-sistance.The longer duration of hospital stay in diabeticpatients can be attributed to the control of glucoselevels rather than to the resolution of infection.

Contrary to the popular belief that diabetic patientsve different causative organisms and need a broaderectrum of antibiotics in management of maxillofacialace infections, the authors wish to defer because of

presented findings.

e authors sincerely thank Dr. Y. S. Rai Dean and Dr.anjan Kumar, Medical Director, S.D.M College ofdical Sciences and Hospital, Dharwad, for allowing ususe the facilities required for the study. The authorsuld also like to thank Dr. S. Amur and Dr. V. K. Joshiproviding their expert advice throughout the course ofstudy. The contribution of Dr. S. Gokul in formattingarticle is sincerely appreciated.

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sis on diabetic patients and repetitive infections. J Infect2005;50(1):34-40.

3. Peters ES, Fong B, Wormuth DW, Sonis ST. Risk factors affect-ing hospital length of stay in patients with odontogenic maxil-lofacial infections. J Oral Maxillofac Surg 1996;54(12):1386-91.; discussion 1391-2.

4. Topazian RG, Goldberg MH, Hupp JR. Oral and maxillofacialinfections. 4th edition. Philadelphia, PA: W.B. Saunders: 2002.

5. Shah BR, Hux JE. Quantifying the risk of infectious diseases forpeople with diabetes. Diabetes Care 2003;26(2):510-3.

6. Huang TT, Tseng FY, Liu TC, Hsu CJ, Chen YS. Deep neckinfection in diabetic patients: comparison of clinical picture andoutcomes with non-diabetic patients. Otolaryngol Head NeckSurg 2005;132(6):943-7.

7. Chen MK, Wen YS, Chang CC, Lee HS, Huang MT, Hsiao HC.Deep neck infections in diabetic patients. Am J Otolaryngol2000;21(3):169-73.

8. Haug RH, Hoffman MJ, Indresano AT. An epidemiologic andanatomic survey of odontogenic infections. J Oral MaxillofacSurg 1991;49(9):976-80.

9. Rega AJ, Aziz SR, Ziccardi VB. Microbiology and antibioticsensitivities of head and neck space infections of odontogenicorigin. J Oral Maxillofac Surg 2006;64(9):1377-80.

10. Stoeckle M, Kaech C, Trampuz A, Zimmerli W. The role ofdiabetes mellitus in patients with bloodstream infections. SwissMed Wkly 2008;138(35-36):512-9.

11. McManus LM, Bloodworth RC, Prihoda TJ, Blodgett JL, Pinck-

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16. Sato FR, Hajala FA, Freire Filho FW, Moreira RW, de MoraesM. Eight-year retrospective study of odontogenic origin infec-tions in a post graduation program on oral and maxillofacialsurgery. J Oral Maxillofac Surg 2009;67(5):1092-7.

17. Pottumarthy S, Fritsche TR, Sader HS, Stiwell MG, Jones RN.Susceptibility patterns of Streptococcus pneumoniae isolate inNorth America (2002-2003): contemporary in vitro activities ofamoxicillin/ clavulanate and 15 other antimicrobial agents. Int JAntimicrob Agents 2005;25:282-9.

18. Har-El G, Aroesty JH, Shaha A, Lucente FE. Changing trends indeep neck abscess. A retrospective study of 110 patients. OralSurg Oral Med Oral Pathol 1994;77(5):446-50.

19. Al-Qamachi LH, Aga H, McMahon J, Leanord A, HammersleyN. Microbiology of odontogenic infections in deep neck spaces:a retrospective study. Br J Oral Maxillofac Surg 2010;48(1):37-9.

20. Carton JA, Maradona JA, Nuo FJ, Fernandez-Alvarez R, Prez-Gonzalez F, Asensi V. Diabetes mellitus and bacteraemia: acomparative study between diabetic and non-diabetic patients.Eur J Med 1993;2(1):62-3.

21. Krishnan V, Johnson JV, Helfrick JF. Management of maxillo-facial infections: a review of 50 cases. J Oral Maxillofac Surg1993;51(8):868-73.; discussion 873-4.

22. Peralta G, Sanchez MB, Roiz MP, Garrido JC, Teira R, Mateos

Rep

DipPosDeS.DSatKadrd

OOOOEe12 Rao et al. October 2010ard RN. Agonist-dependent failure of neutrophil function indiabetes correlates with extent of hyperglycemia. J Leukoc Biol2001;70(3):395-404.Storoe W, Haug RH, Lillich TT. The changing face of odonto-genic infections. J Oral Maxillofac Surg 2001;59(7):739-48.Wang J, Ahani A, Pogrel MA. A five-year retrospective study ofodontogenic maxillofacial infections in a large urban publichospital. Int J Oral Maxillofac Surg 2005;34:646-649.Youssef W, DInnocenzo R, Mehra P. Antibiotic therapy in themanagement of severe odontogenic infections: a comparison oftwo treatment regimens. Oral Surg Oral Med Oral Pathol OralRadiol Endod 2008;106(4):505.F. Diabetes does not affect outcome in patients with Enterobac-teriaceae bacteremia. BMC Infect Dis 2009;9:94.

rint requests:

esh D. Rao, MDStgraduate

partment of Oral and Maxillofacial Surgery.M College of Dental Sciences and Hospitaltur, Dharwadrnataka, Indiaipesh.rao@gmail.com

Comparison of maxillofacial space infection in diabetic and nondiabetic patientsPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONACKNOWLEDGMENTREFERENCES