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Periodontal Disease as a Primary Cause of Surgical Site Infection in Fractures of the Mandible – is smoking a confounding variable?

Open AccessPublished:August 12, 2022DOI:https://doi.org/10.1016/j.bjoms.2022.08.001

      Abstract

      Fractures of the mandible are common in contemporary Oral and Maxillofacial Practice. Wound infection is the most common complication after open reduction and internal fixation and the management of these is complex and costly in terms of morbidity to the patient and in fiscal terms. Whilst numerous epidemiological studies implicate smoking, alcohol, drug use, adverse behaviour as well as fracture complexity and diabetes as important risk factors, the role of periodontal disease is only occasionally mentioned and not formally investigated.
      The aim of this study was to assess the presence of periodontal disease and severity according to the 2018 EFP/AAP periodontitis case classification in a population of patients with fractured mandibles presenting to a single level 1 trauma centre, and to look for a possible association with surgical site infection.
      A total of 305 patients were assessed retrospectively following open reduction and internal fixation via transoral incisions with load sharing osteosynthesis . The post-operative infection rate was 22.95%.
      Statistical analysis using multivariate and multiple logistic regression revealed that there was a strong association between periodontal staging and post-operative surgical site infection.
      Crucially the study predicts that patients with severe periodontal disease (periodontal stage III and IV) are over 7 times more likely to develop wound infection than disease negative individuals. This has implications in risk adjustment, prognostication, treatment planning, and post-operative care. Surprisingly in this study cigarette smoking did not achieve statistical significance as it is an established risk factor in the pathogenesis of periodontal disease, potentially conflicting with established literature.

      Keywords

      Introduction

      Fractures of the mandible are common in facial trauma practice and management has undergone a stepwise evolution following increased understanding and advances in surgical materials. Operative surgery is now focused upon open reduction and internal fixation conducted through transoral incisions. Whilst this surgery has predictable outcomes it is not without risk of complications which could vary and be categorized as wound infection, wound dehiscence, non-union, osteomyelitis, nerve damage, and malocclusion. Wound infection was the most common complication after open reduction and internal fixation and accounted for up to one-third of all complications encountered [
      • Lamphier J.
      • Ziccardi V.
      • Ruvo A.
      • et al.
      Complications of mandibular fractures in an urban teaching center.
      ].
      Infections of plates like in orthopaedics occur with the establishment of an oral biofilm which is highly predictive of plate failure [
      • Jhass A.K.
      • Johnston D.A.
      • Gulati A.
      • et al.
      A scanning electron microscope characterisation of biofilm on failed craniofacial osteosynthesis miniplates.
      ]. The precise microbiology of infected fractures is not established. Management of the infected miniplate is confusing as the literature does not distinguish between mucosal dehiscence and established infection with biofilm [
      • Cahill 3rd, T.J.
      • Gandhi R.
      • Allori A.C.
      • et al.
      Hardware Removal in Craniomaxillofacial Trauma: A Systematic Review of the Literature and Management Algorithm.
      ], but the management of an established infected fracture requires definitive hardware removal, debridement, and load-bearing osteosynthesis [
      • Mehra P.
      • Van Heukelom E.
      • Cottrell D.A.
      Rigid internal fixation of infected mandibular fractures.
      ].
      Historically, there have been several published reports looking at risk factors for poor outcomes which are described in several ways. Smoking is frequently cited as a common risk factor and microbial biofilm was also linked to the chronic infections associated with failed craniofacial osteosynthesis plates. Confocal microscopy identified 75% of the plates exhibited evidence of biofilm to varying degrees [
      • Jhass A.K.
      • Johnston D.A.
      • Gulati A.
      • et al.
      A scanning electron microscope characterisation of biofilm on failed craniofacial osteosynthesis miniplates.
      ].
      Periodontitis is a chronic multifactorial inflammatory disease associated with dysbiotic plaque biofilms and characterized by progressive destruction of the tooth-supporting apparatus [
      • Papapanou P.N.
      • Sanz M.
      • Buduneli N.
      • et al.
      Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions.
      ]. The recently introduced 2018 EFP/AAP periodontitis case classification of periodontal disease allows clinicians to identify clinical entities and facilitate the process of treatment planning. [
      • Tonetti M.S.
      • Greenwell H.
      • Kornman K.S.
      Staging and grading of periodontitis: Framework and proposal of a new classification and case definition.
      ]. Clinical attachment and marginal alveolar bone loss have remained the key features to classify the severity of periodontitis which share similar features to that of infected fractures.
      Given that periodontal disease can be quantified the hypothesis is postulated that severity of the disease can be predictive of fracture failure. Therefore, the aim of this present study was to assess periodontal disease using the 2018 EFP/AAP periodontitis case classification among patients with mandibular fractures in relation to mandibular fracture.

      Material and Methods

      A retrospective analysis was conducted at Royal London Hospital. Data were collected from clinical records and the radiographs from picture archiving and communication system (PACS) of patients with mandibular fractures admitted for surgical management using intra oral incisions and load sharing osteosynthesis between 2017 and 2020. Exclusion criteria included patients under the age of 18, patients with isolated mandibular condylar process fractures, edentulous fractures, fracture patterns requiring load bearing reconstructions with or without preexisting infections, and patients with incomplete clinical or radiological data. Details of patient’s information, including physical status (ASA) classification, smoking and homelessness were obtained. Panoramic radiographs were also analyzed. Radiographic assessments were performed to obtain the following information: Figure 1, Figure 2.
      • 1)
        periodontal staging [
        • Tonetti M.S.
        • Greenwell H.
        • Kornman K.S.
        Staging and grading of periodontitis: Framework and proposal of a new classification and case definition.
        ]
      • 2)
        periodontal grading [
        • Tonetti M.S.
        • Greenwell H.
        • Kornman K.S.
        Staging and grading of periodontitis: Framework and proposal of a new classification and case definition.
        ]
      • 3)
        extent of periodontitis [
        • Sanz M.
        • Papapanou P.N.
        • Tonetti M.S.
        • et al.
        Guest Editorial: Clarifications on the use of the new classification of periodontitis. Wiley Online.
        ]
      • 4)
        the number of remaining teeth
      Figure thumbnail gr1
      Figure 1An example of radiographic assessment in patient without post-operative infection
      Figure thumbnail gr2
      Figure 2An example of radiographic assessment in patient with post- operative infection subsequently treated with a load bearing osteosynthesis – the subsequent healing and union was uneventful
      Details of the modified criteria for data collection is shown in Table 1. . Examples of radiographic assessment in mandibular fracture patients without and with post-operative infection are illustrated in figure 1 and figure 2, respectively.
      Table 1The modified criteria
      Measure0123
      Periodontitis stageNo bone lossBone loss <15% (stage I)Bone loss 15-33% (stage II)Extending to middle third of root or beyond (stage III & IV)
      Periodontitis grade%Bone loss/age <0.25 regardless of smoking status%Bone loss/age 0.25-1.0 or smokers%Bone loss/age > 1.0 regardless of smoking status
      Periodontitis extentLocalised < 30%Generalised ≥30%
      Number of teeth present≥ 20 teeth with 10 opposing pairs≥ 20 teeth without 10 opposing pairs< 20 teeth without 10 opposing pairs
      Teeth in line of fractureNot associated or teeth were already removedAssociated with teeth without diseaseAssociated with teeth with periodontal disease or dental caries
      The presence of infection was recorded from the notes and included physical signs of pathological swelling, gross wound dehiscence, pathological sinus, presence of pus at site of repair, and observation of gross granulation tissue at the incision line.
      Statistical analyses were performed using IBM SPSS statistics (version 27.0 Inc., New York, NY, USA). The level of significance was set at 0.05. Bivariate analysis using Chi-square test were performed to test the statistical significance of risk factors and infection. Variables that were statistically significant were subsequently subjected to multiple logistic regression to predict the rate of infection.

      Results

      Table 2
      Table 2Results
      CategoryOutcome
      Sample (N)305
      Gender (male)261 (85.6%)
      Age median (range)
      All subjects29 (18-90)
      Male28 (18-82)
      Female33 (18-90)
      Infection70 (22.95%)
      Physical status
      ASA I162 (53.1%)
      ASA II125 (41.0%)
      ASA III13 (4.3%)
      Smokers197 (64.6%)
      Homelessness20 (6.6%)
      Patients with periodontitis179 (58.69%)
      Periodontal stage
      Periodontitis stage I46 (15.1%)
      Periodontitis stage II81 (26.6%)
      Severe periodontitis (stage III/IV)52 (17%)
      Periodontal grade
      Periodontitis grade A9 (5%)
      Periodontitis grade B113 (63.1%)
      Periodontitis grade C57 (31.8%)
      Number of teeth
      ≥ 20 teeth & ≥ 10 opposing pairs266 (68.6%)
      ≥ 20 teeth & < 10 opposing pairs23 (5.9%)
      < 20 teeth & < 10 opposing pairs15 (3.9%)
      Teeth in line of fracture
      No teeth in line of fracture70 (18%)
      Teeth free of pathology in line of fracture190 (49%)
      Tooth with pathology in line of fracture45 (11.6%)
      A total of 388 patients with a fracture of the mandible were admitted for operative intervention between 2017 and 2020 . Of these, 305 patients were included in the analysis following application of exclusion criteria.
      The median age of patients was 29 years (ranging from 18 to 90 years), and the majority of patients were male (85.6%). Seventy patients experienced infection with an overall infection rate of 22.95%. Confirmed smokers, non-smokers, and patients with unknown smoking status were found in 197 (64.6%), 74 (24.3%), and 34 (11.1%), respectively.
      126 out of 305 patients did not have diagnosable periodontal disease, while 179 patients had an objective degree of periodontitis. Staging of periodontitis was assessed as Severe (Periodontal stage III and IV) in 52 (17%) out of all periodontitis patients. The number of patients that were graded as A, B, and C were 9 (5%), 113 (32%), and 57 (63%), respectively. There were 266 (68.6%) patients who presented with ≥20 remaining teeth with 10 opposing pairs, 23 (5.9%) of patients presented with ≥20 remaining teeth without 10 opposing pairs, and 15 patients (3.9%) presented with <20 remaining teeth without 10 opposing pairs. Regarding teeth in the line of plates, 70 (18%) of patients presented with no association of line of plates and teeth, 190 (49%) of patients presented with teeth associated with the line of plates but without signs of pathologies of associated teeth, and 45 of patients (11.6%) presented with teeth associated with the line of plates with signs of pathologies including periodontitis and dental caries.
      Bivariate analysis using Chi-squared tests indicated that there were statistical associations between physical status (ASA classification), homelessness, periodontal stage, periodontal grade, periodontal extent and mandibular fracture with post-operative infection (Table 3). The results from logistic regression analysis (Table 4) showed that only periodontal stage remained statistically significant (p <0.001) in the final model. The odds ratio (95% CI) of periodontal stage III/IV was 7.169 (2.952-17.410) (p<0.001), supporting our observation that it was those patients with extensive periodontal disease who were most susceptible for wound infection.
      Table 3Bivariate analysis on (possible) risk factors and plate infection (Chi-square test)
      FactorP-value
      Gender0.942
      ASA0.019*
      Smoking0.427
      Homelessness0.01*
      Periodontal stage<0.001**
      Periodontal grade
      In patients with periodontitis only
      <0.001**
      Periodontal extent
      In patients with periodontitis only
      <0.001**
      Number of teeth0.318
      Teeth in line of fracture0.092
      *p<0.05
      **p<0.001
      In patients with periodontitis only
      Table 4Final model of logistic regression analysis on the risk factors and plate infection.
      FactorEstimate (SE)Odds ratio (95% CI)p-value
      Periodontal stage<0.001**
      No detectable bone loss
      Reference category
      Periodontal stage I0.802 (0.510)2.230 (0.821-6.060)0.116
      Periodontal stage II0.620 (0.451)1.859 (0.767-4.501)0.170
      Periodontal stage III/IV1.970 (0.453)7.169 (2.952-17.410)<0.001**
      Constant-2.124 (0.319)<0.001**
      **p<0.001
      a Reference category

      Discussion

      The Royal London Hospital is a level one trauma centre and is situated in a poor socioeconomic area with a significant case mix volume of both routine and complex facial trauma. The high mandibular infection rate of 23% is reflected in other studies involving inner city populations with adversarial co- factors such as alcohol, drug, substance abuse, and poor health and social measures [
      • Haug R.H.
      • Serafin B.L.
      Mandibular Angle Fractures: A Clinical and Biomechanical Comparison-the Works of Ellis and Haug.
      ]. Historically in addition to social and behavioural factors [
      • Hsieh T.Y.
      • Funamura J.L.
      • Dedhia R.
      • et al.
      Risk Factors Associated With Complications After Treatment of Mandible Fractures.
      ,
      • Hurrell M.J.L.
      • David M.C.
      • Batstone M.D.
      Patient compliance and mandible fractures: a prospective study.
      ,
      • Marciani R.D.H.J.
      • Kohn M.W.
      Patient compliance - a risk factor in facial trauma repair.
      ], site of fracture and complexity [
      • Lamphier J.
      • Ziccardi V.
      • Ruvo A.
      • et al.
      Complications of mandibular fractures in an urban teaching center.
      ,

      Luz JGC MR, DAliva RP, Yamamotoo MK. Factors contributing to the surgical retretment of mandibular fractures. Braz Oral Res. 2013;27.

      ], medical co factors [
      • Raikundalia M.
      • Svider P.F.
      • Hanba C.
      • et al.
      Facial fracture repair and diabetes mellitus: An examination of postoperative complications.
      ], time to surgery [
      • Malanchuk V.O.
      • Kopchak A.V.
      Risk factors for development of infection in patients with mandibular fractures located in the tooth-bearing area.
      ], experience of surgeon [

      Mathog RH, Toma V, Clayman L et al. Nonunion of the mandible: an analysis of contributing factors. J Oral Maxillofac Surg. 2000;58(7):746-52; discussion 52-3.

      ] and even types of plating strategy [
      • Laverick S.
      • Siddappa P.
      • Wong H.
      • et al.
      Intraoral external oblique ridge compared with transbuccal lateral cortical plate fixation for the treatment of fractures of the mandibular angle: prospective randomised trial.
      ] are quoted. In almost all studies smoking is universally implicated as the primary factor in plate infection and subsequent failure, and yet despite the well-recognised role of tobacco in primary pathogenesis of periodontal disease [
      • Leite F.R.M.
      • Nascimento G.G.
      • Scheutz F.
      • et al.
      Effect of Smoking on Periodontitis: A Systematic Review and Meta-regression.
      ], the formal association between periodontal disease and fracture infection in a dose dependent manner remains unproven until now.
      Severe periodontitis affects around 11.2% of the population globally, representing the sixth-most prevalent condition in the world [
      • Kassebaum N.J.
      • Bernabe E.
      • Dahiya M.
      • et al.
      Global burden of severe periodontitis in 1990–2010: a systematic review and meta-regression.
      ]. Epidemiological studies indicate that the prevalence of periodontitis increases among male patients, patients with low educational and income levels, and smokers [
      • Eke P.I.
      • Borgnakke W.S.
      • Genco R.J.
      Recent epidemiologic trends in periodontitis in the USA.
      ,
      • Genco R.J.
      • Borgnakke W.S.
      Risk factors for periodontal disease.
      ]. The high prevalence of periodontitis in this study was observed despite relatively young patients which may be explained by the fact that the Hospital is situated in a poor socioeconomic area as well as the majority of the patients were male and smokers [
      • Grossi S.G.
      • Zambon J.J.
      • Ho A.W.
      • Koch G.
      • et al.
      Assessment of risk for periodontal disease. I. Risk indicators for attachment loss.
      ]. The extent of dental disease within our catchment area was evidenced by the Tower Hamlets Joint Strategic Needs Assessment of 2015 whereby 39% of adults had decayed teeth and 77% had periodontal disease[

      https://www.towerhamlets.gov.uk/Documents/Public-Health/JSNA/JSNA_Summary.pdf July 2022

      ].
      The prevalence of periodontitis and its severity classified by the 2018 EFP/AAP classification found in this study was in line with a previous study. In this study, 26.6% and 17% of patients were diagnosed with stage II and III&IV respectively, which is comparable to 24.6% and 19.7% in Germen’s study [
      • Germen M.
      • Baser U.
      • Lacin C.C.
      • et al.
      Periodontitis Prevalence, Severity, and Risk Factors: A Comparison of the AAP/CDC Case Definition and the EFP/AAP Classification.
      ]. Patients who were classified with periodontal stage III and IV were much more likely to experience a post-operative infection with the odds of up to 7-fold (OR:7.17, 95% CI:2.95-17.41) compared to patients with no detectable periodontal bone loss. Periodontitis stages I and II showed an increasing rate of post-operative infection compared to patients with no detectable periodontal disease although they were not statistically significant (p=0.116 and 0.170, respectively). These findings strongly highlighted periodontal disease as an important risk indicator affecting post-operative infection rate among patients with mandibular fractures.
      The results of the present study indicated the periodontal disease using 2018 EFP/AAP classification could potentially be an important screening tool to predict the rate of complication after treatment of a mandibular fracture, this observation also is important in risk adjustment of outcome and almost certainly explains the higher rates of infection in inner city populations with poor health behaviors.
      Grading reflects the patient’s susceptibility to periodontal disease as well as indicates the presence of risk factors (e.g., smoking and diabetes). This study utilized mainly the ratio of the percentage of bone loss/age as a key determinant to define grading as it also had been suggested to be the most pragmatic to reflect the average rate of disease progression over time [
      • Dietrich T.
      • Ower P.
      • Tank M.
      • et al.
      Periodontal diagnosis in the context of the 2017 classification system of periodontal diseases and conditions–implementation in clinical practice.
      ]. More than half of the patients (63.1%) were classified with grade B, this was due to either displaying the percentage of bone loss per age >0.25-1 or their smoking status. The fact that up to one-third of the patients in this study were classified as grade C, indicating that a substantial proportion of patients with mandibular fractures showed a rapid rate of periodontal progression [
      • Tonetti M.S.
      • Greenwell H.
      • Kornman K.S.
      Staging and grading of periodontitis: Framework and proposal of a new classification and case definition.
      ].
      Tobacco smoking, which was recently suggested to be a nicotine-dependent condition and chronic relapsing medical disorder, is an important risk factor for periodontal disease [
      • Jepsen S.
      • Caton J.G.
      • Albandar J.M.
      • et al.
      Periodontal manifestations of systemic diseases and developmental and acquired conditions: Consensus report of workgroup 3 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions.
      ]. This important modifying factor increases the risk of periodontal disease and results in higher rate of tooth loss [
      • Genco R.J.
      • Borgnakke W.S.
      Risk factors for periodontal disease.
      ,
      • Warnakulasuriya S.
      • Dietrich T.
      • Bornstein M.M.
      • et al.
      Oral health risks of tobacco use and effects of cessation.
      ,
      • Tomar S.L.
      • Asma S.
      Smoking-attributable periodontitis in the United States: findings from NHANES III.
      ]. The detrimental effect of smoking could be observed in the alteration of microbial community toward dysbiosis, effects on neutrophil function toward a more destructive direction, and the impairment of vasculature and periodontal healing by affecting fibroblast function [
      • Palmer R.M.
      • Wilson R.F.
      • Hasan A.S.
      • et al.
      Mechanisms of action of environmental factors–tobacco smoking.
      ]. Smoking was also cited as the important risk factor associated with an increased complication rate among patients treated for mandibular fracture [
      • Hsieh T.Y.
      • Funamura J.L.
      • Dedhia R.
      • et al.
      Risk Factors Associated With Complications After Treatment of Mandible Fractures.
      ,
      • Gutta R.
      • Tracy K.
      • Johnson C.
      • et al.
      Outcomes of mandible fracture treatment at an academic tertiary hospital: a 5-year analysis.
      ,
      • Furr A.M.
      • Schweinfurth J.M.
      • May W.L.
      Factors associated with long-term complications after repair of mandibular fractures.
      ]. Most of the patients (64.6%) in this present study were smokers. Nevertheless, smoking had failed to show a significant association with mandibular fracture infection. This was in line with a recent finding by Oksa et al. (2022) demonstrating that smoking also failed to show a significant association with infection after treatment of mandibular fracture [
      • Oksa M.
      • Haapanen A.
      • Marttila E.
      • et al.
      Simple dentate area fractures of the mandible–can we prevent postoperative infections?.
      ]. Moreover, periodontal disease as part of tooth index was utilized in that study, which also include dental caries and apical periodontitis. Thus, the true effect of periodontal disease and the association with mandibular fracture infection may be confounded by other dental-related factors.
      Most of the patients in this present study were classified to ASA class I or II, indicating healthy patients or patients with only mild systemic disease were included in the analysis. Homelessness was common (6.6%) which possess a higher risk for oral and dental disease as well as limited access to dental and medical care. Both of these factors were significant on univariate analysis, but not in the final model. Periodontal disease is certainly exacerbated by ill health and also frequently see in the homeless. The strength of the association of periodontal staging possibly reduced the significance of these two factors. [

      Simons D, Pearson N, Movasaghi Z. Developing dental services for homeless people in East London. British Dental Journal. 2012;213(7):E11-E.

      ].
      This retrospective study is not without limitations particularly as periodontal status was determined radiologically rather than clinically. However in mitigation it has been suggested that radiographic bone loss could be used for periodontitis staging/grading assessment with caution in that radiographs may underestimate the loss of interdental bone [
      • Christiaens V.
      • De Bruyn H.
      • Thevissen E.
      • et al.
      Assessment of periodontal bone level revisited: a controlled study on the diagnostic accuracy of clinical evaluation methods and intra-oral radiography.
      ] meaning that patients may have more severe periodontal disease than what was detected on panoramic radiographs. Despite a possibility of underestimation of periodontal bone loss by radiographic examination, plate infections were still found to be highly correlated with the stage of periodontal disease.

      Conclusion

      The prognostication and therapeutic implications of linking periodontal status with fracture healing are obvious, and a prospective study to include clinical assessment of periodontal disease is obvious and relationship to other published risk factors is underway and remain to be further investigated.
      Ethics statement/confirmation of patient permission
      The local ethics committee (Bartshealth NHS Trust and QMUL) were approached and passed the study as low risk. Patient permission obtained

      Acknowledgement

      The authors gratefully acknowledge Madeline J. Y. Yon for statistical analysis.

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