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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, and 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 therefore was to assess the presence of periodontal disease and its severity according to the 2018 EFP/AAP periodontitis case classification in patients with fractured mandibles who presented 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 postoperative infection rate was 22.95%. Multivariate and multiple logistic regression revealed that there was a strong association between periodontal staging and postoperative surgical site infection. Crucially, the study predicts that patients with severe periodontal disease (periodontal stage III and IV) are over seven times more likely to develop a wound infection than disease-negative individuals. This has implications for risk adjustment, prognostication, treatment planning, and postoperative care. Surprisingly in this study, cigarette smoking, an established risk factor in the pathogenesis of periodontal disease, did not achieve statistical significance, potentially conflicting with the 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 on open reduction and internal fixation through transoral incisions. Whilst this has predictable outcomes it is not without risk of complications, which can vary and be categorised 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 the complications encountered.
      • Lamphier J.
      • Ziccardi V.
      • Ruvo A.
      • et al.
      Complications of mandibular fractures in an urban teaching center.
      Infections of plates occur (as in orthopaedics) 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 yet established. Management of the infected miniplate is confusing, as the literature does not distinguish between mucosal dehiscence and established infection with biofilm,
      • Cahill III, 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, several published reports have looked at risk factors for poor outcomes, which are described in several ways. Smoking is frequently cited as a common risk factor, and microbial biofilm has been linked to chronic infections associated with failed craniofacial osteosynthesis plates. Confocal microscopy showed that 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 that is associated with dysbiotic plaque biofilms and characterised 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 European Federation of Periodontology (EFP)/American Academy of Periodontology (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, which share similar features to those of infected fractures, have remained the key features with which to classify the severity of periodontitis.
      Given that periodontal disease can be quantified, the hypothesis is postulated that the severity of the disease can be predictive of fracture failure. The aim of this present study therefore was to assess periodontal disease using the 2018 EFP/AAP periodontitis case classification among patients with mandibular fractures.

      Material and methods

      A retrospective analysis was conducted at the Royal London Hospital. Data on patients admitted between 2017 and 2020 for surgical management of mandibular fractures using intraoral incisions and load-sharing osteosynthesis were collected from clinical records. Radiographs were collected from the picture archiving and communication system (PACS). Exclusion criteria included patients under the age of 18, those with isolated mandibular condylar process fractures, edentulous fractures, fracture patterns requiring load-bearing reconstructions with or without pre-existing infections, and those with incomplete clinical or radiological data. Details of patients’ information, including physical status (American Society of Anesthesiologists, ASA) classification, smoking, and homelessness were obtained. Panoramic radiographs were also analysed. Radiographic assessments were performed to obtain the following information (Fig. 1, Fig. 2): 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.
      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.
      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.
      and number of remaining teeth.
      Figure thumbnail gr1
      Fig. 1Example of radiographic assessment in a patient without postoperative infection.
      Figure thumbnail gr2
      Fig. 2Example of radiographic assessment in a patient with a postoperative infection subsequently treated with a load-bearing osteosynthesis. The subsequent healing and union were uneventful.
      Details of the modified criteria for data collection are shown in Table 1. Examples of the radiographic assessment of mandibular fracture patients with and without postoperative infection are illustrated in Fig. 1, Fig. 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 (stages 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 extent-Localised < 30%Generalised ≥30%-
      Number of teeth present≥ 20 teeth with10 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-
      Presence of infection was recorded from the notes and included physical signs of pathological swelling, gross wound dehiscence, pathological sinus, presence of pus at the site of repair, and observation of gross granulation tissue at the incision line.
      Statistical analyses were performed using IBM SPSS Statistics for Windows version 27.0 (IBM Corp). The level of statistical significance was set at 0.05. Bivariate analyses using the chi-squared 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 presence of infection.

      Results

      A total of 388 patients with a fracture of the mandible were admitted for operative intervention between 2017 and 2020. Of these, 305 were included in the analysis following application of the exclusion criteria (Table 2).
      Table 2Results. Data are number (%) unless otherwise stated.
      CategoryOutcome
      Sample (N)305
      Gender (male)261(85.6)
      Median (range) age (years):
       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:
        I46 (15.1)
       II81 (26.6)
       III/IV (severe periodontitis)52 (17)
      Periodontitis grade:
       A9 (5)
       B113 (63.1)
       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)
      The median (range) age of the patients was 29 (18 - 90) years, and the majority were male (85.6%). Seventy patients experienced infection, with an overall infection rate of 22.95%. Confirmed smokers, non-smokers, and patients with an unknown smoking status were found in 197 (64.6%), 74 (24.3%), and 34 (11.1%), respectively.
      Of 305 patients, 126 did not have diagnosable periodontal disease, while 179 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 graded as A, B, and C were 9 (5%), 113 (32%), and 57 (63%), respectively. A total of 266 (68.6%) patients presented with ≥20 remaining teeth with 10 opposing pairs, 23 (5.9%) presented with ≥20 remaining teeth without 10 opposing pairs, and 15 (3.9%) presented with<20 remaining teeth without 10 opposing pairs. Regarding teeth in the line of plates, 70 patients (18%) presented with no association of line of plates and teeth, 190 (49%) presented with teeth associated with the line of plates but without signs of pathology of associated teeth, and 45 (11.6%) presented with teeth associated with the line of plates and signs of pathology including periodontitis and dental caries.
      Bivariate analysis using chi-squared tests indicated that there were statistically significant associations between physical status (ASA classification), homelessness, periodontal stage, periodontal grade, periodontal extent, and mandibular fracture with postoperative infection (Table 3). Results from the multivariate logistic regression analysis (Table 4) showed that only periodontal stage remained statistically significant (p<0.001) in the final model. The R2of the final model was 0.12. The odds ratio (95% CI) of periodontal stage III/IV was 7.17 (2.95 to 17.41) (p<0.001), supporting our observation that it was patients with extensive periodontal disease who were most susceptible to wound infection relative to patients with no detectable bone loss.
      Table 3Bivariate analysis on (possible) risk factors and plate infection (chi-squared test).
      FactorValuedfp value
      Gender0.0510.942
      ASA7.97820.019
      Smoking0.63210.427
      Homelessness6.56510.01
      Periodontal stage38.2583<0.001
      Periodontal grade
      In patients with periodontitis only.
      30.0523<0.001
      Periodontal extent
      In patients with periodontitis only.
      17.0282<0.001
      Number of teeth2.29320.318
      Teeth in line of fracture4.77520.092
      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
      p<0.001.
       No detectable bone loss
      Reference category.
      ---
       Stage I0.802 (0.510)2.230 (0.821 to 6.060)0.116
       Stage II0.620 (0.451)1.859 (0.767 to 4.501)0.170
       Stage III/IV1.970 (0.453)7.169 (2.952 to 17.410)<0.001
      p<0.001.
      Constant-2.124 (0.319)-<0.001
      p<0.001.
      R2 = 0.122; SE: standard error; 95% CI: 95% confidence interval.
      a Reference category.
      ** p<0.001.

      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 routine and complex facial trauma. The high mandibular infection rate of 23% is reflected in other studies involving inner city populations with adversarial cofactors such as alcohol, drug and 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.
      • David M.C.
      • Batstone M.D.
      Patient compliance and mandible fractures: a prospective study.
      • Marciani R.D.
      • Haley J.V.
      • 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 J.G.
      • Moraes R.B.
      • D'Ávila R.P.
      • et al.
      Factors contributing to the surgical retreatment of mandibular fractures.
      medical cofactors,
      • 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 the surgeon,
      • Mathog R.H.
      • Toma V.
      • Clayman L.
      • et al.
      Nonunion of the mandible: an analysis of contributing factors.
      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.
      have been quoted. In almost all studies smoking is universally implicated as the primary factor in plate infection and subsequent failure, yet despite the well-recognised role of tobacco in the primary pathogenesis of periodontal disease,
      • Leite F.R.
      • 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 has remained 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.
      • Bernabé 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, those 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 despite patients being relatively young may be explained by the fact that the hospital is situated in a poor socioeconomic area and by the fact that the majority were male and smokers.
      • Grossi S.G.
      • Zambon J.J.
      • Ho A.W.
      • 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, which found that 39% of adults had decayed teeth and 77% had periodontal disease.

      Joint strategic needs assessment: summary document. Life, health, and wellbeing in Tower Hamlets, November 2016. Available from URL: https://www.towerhamlets.gov.uk/Documents/Public-Health/JSNA/JSNA_Summary.pdf (last accessed 23 August 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 our study 26.6% and 17% of patients were diagnosed with stage II and stages III and IV, respectively, which is comparable to 24.6% and 19.7% in the study by Germen et al.
      • 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 stages III and IV were much more likely to experience a postoperative infection with an odds ratio up to seven-fold (OR:7.17, 95% CI: 2.95 to 17.41) compared with patients with no detectable periodontal bone loss. Patients with periodontitis stages I and II showed an increasing rate of postoperative infection compared with those with no detectable periodontal disease, although these were not statistically significant (p=0.116 and 0.170, respectively). These findings strongly highlight periodontal disease as an important risk indicator affecting the postoperative infection rate among patients with mandibular fractures.
      The results of the present study have shown that the 2018 EFP/AAP classification of periodontal disease could potentially be an important screening tool to predict the rate of complication after treatment of a mandibular fracture. This observation is also important for the risk adjustment of outcome, and almost certainly explains the higher rates of infection in inner city populations with poor health behaviours.
      Grading reflects the patient’s susceptibility to periodontal disease and indicates the presence of risk factors such as smoking and diabetes. This study mainly utilised the ratio of the percentage of bone loss/age as a key determinant to define grading, as it has also been suggested as being 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 the patients (63.1%) were classified as grade B, which was due to the percentage of bone loss/age of >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 indicated that a substantial proportion of those 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 a 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 an alteration of the microbial community towards dysbiosis, an effect on neutrophil function to a more destructive direction, and the impairment of vasculature and periodontal healing through an effect on 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 an important risk factor associated with an increased complication rate among patients treated for mandibular fractures.
      • 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 failed to show a significant association with mandibular fracture infection. This is in line with a recent finding by Oksa et al
      • Oksa M.
      • Haapanen A.
      • Marttila E.
      • et al.
      Simple dentate area fractures of the mandible–can we prevent postoperative infections?.
      who also found that smoking failed to show a significant association with infection after the treatment of mandibular fractures.
      • 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 the tooth index, which also includes dental caries and apical periodontitis, was utilised in that study. 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 as ASA class I or II, indicating that healthy patients or those with only mild systemic disease were included in the analysis. Homelessness was common (6.6%), and these patients possess a higher risk of oral and dental disease as well as limited access to dental and medical care. Both these factors were significant on univariate analysis, but not in the final model. Periodontal disease is certainly exacerbated by ill health that is frequently seen 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.
      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, as 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 is detected on panoramic radiographs. Despite the possibility of radiographic examination underestimating periodontal bone loss, plate infections still highly correlated with the stage of periodontal disease.

      Conclusion

      The prognostic and therapeutic implications of linking periodontal status with fracture healing are obvious. A prospective study to include the clinical assessment of periodontal disease and the relation to other published risk factors is underway and remains to be further investigated.

      Ethics statement/confirmation of patient permission

      The local ethics committee (Bartshealth NHS Trust and QMUL) was approached and passed the study as low risk. Patients’ permission obtained.

      Conflict of interest

      There are no conflicts of interest.

      Acknowledgement

      The authors gratefully acknowledge Madeline JY Yon for statistical analysis.

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