Relationship between 18F-FDG Uptake in the Oral Cavity, Recent Dental Treatments, and Oral Inflammation or Infection: A Retrospective Study of Patients with Suspected Endocarditis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Patients
2.2. Status Praesens, Oral Health, and Dental Records
2.3. [18F]FDG PET/CT Acquisition and Interpretation
2.4. [18F]FDG PET/CT Scan Analyses of the Oral Cavity and Extra-Cardiac Areas
2.5. Statistical Analyses
3. Results
3.1. Dental Procedures Prior to [18F]FDG PET/CT Imaging
3.2. Oral Status Praesens at Time of [18F]FDG PET/CT Imaging
3.3. Visual [18F]FDG Uptake Scores and SUVmax Compared with Dental Treatments
3.4. Cardiac and Extra-Cardiac [18F]FDG PET/CT Findings
4. Discussion
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
Ethics Approval
References
- Li, X.; Kolltveit, K.M.; Tronstad, L.; Olsen, I. Systemic diseases caused by oral infection. Clin. Microbiol. Rev. 2000, 13, 547–558. [Google Scholar] [CrossRef]
- Loesche, W.J. Association of the oral flora with important medical diseases. Curr. Opin. Periodontol. 1997, 4, 21–28. [Google Scholar] [PubMed]
- Cahill, T.J.; Baddour, L.M.; Habib, G.; Hoen, B.; Salaün, E.; Pettersson, G.B.; Schäfers, H.J.; Prendergast, B.D. Challenges in Infective Endocarditis. J. Am. Coll. Cardiol. 2017, 69, 325–344. [Google Scholar] [CrossRef] [PubMed]
- Lockhart, P.B.; Brennan, M.T.; Thornhill, M.; Michalowicz, B.S.; Noll, J.; Bahrani-Mougeot, F.K.; Sasser, H.C. Poor oral hygiene as a risk factor for infective endocarditis–related bacteremia. J. Am. Dent. Assoc. 2009, 140, 1238–1244. [Google Scholar] [CrossRef] [PubMed]
- Lockhart, P.B.; Brennan, M.T.; Sasser, H.C.; Fox, P.C.; Paster, B.J.; Bahrani-Mougeot, F.K. Bacteremia Associated With Toothbrushing and Dental Extraction. Circulation 2008, 117, 3118–3125. [Google Scholar] [CrossRef] [Green Version]
- Veinot, J.P. Pathologic Findings: Valvular Destruction, Perivalvular Abnormalities, and Extracardiac Findings. In Endocarditis. Diagnosis and Management, 2nd ed.; Chan, K.L., Embil, J.M., Eds.; Springer International Publishing: Heidelberg, Germany, 2016; pp. 9–26. [Google Scholar]
- Parahitiyawa, N.B.; Jin, L.J.; Leung, W.K.; Yam, W.C.; Samaranayake, L.P. Microbiology of odontogenic bacteremia± beyond endocarditis. Clin. Microbiol. Rev. 2009, 22. [Google Scholar] [CrossRef] [Green Version]
- Glenny, A.-M.; Oliver, R.; Roberts, G.J.; Hooper, L.; Worthington, H. Antibiotics for the prophylaxis of bacterial endocarditis in dentistry. Cochrane Database Syst. Rev. 2013, 10, CD003813. [Google Scholar] [CrossRef]
- Habib, G.; Erba, P.A.; Iung, B.; Donal, E.; Cosyns, B.; Laroche, C.; Popescu, B.A.; Prendergast, B.; Tornos, P.; Sadeghpour, A.; et al. Clinical presentation, aetiology and outcome of infective endocarditis. Results of the ESC-EORP EURO-ENDO (European infective endocarditis) registry: A prospective cohort study. Eur. Hear. J. 2019, 40, 3222–3232. [Google Scholar] [CrossRef] [Green Version]
- Navarro, B.G.; Jané-Salas, E.; Estrugo-Devesa, A.; López, J.L.; Viñas, M. Bacteremia Associated With Oral Surgery: A Review. J. Évid. Based Dent. Pract. 2017, 17, 190–204. [Google Scholar] [CrossRef]
- Cahill, T.J.; Prendergast, B.D. Infective endocarditis. Lancet 2016, 387, 882–893. [Google Scholar] [CrossRef] [Green Version]
- Vogkou, C.T.; Vlachogiannis, N.I.; Palaiodimos, L.; Kousoulis, A.A. The causative agents in infective endocarditis: A systematic review comprising 33,214 cases. Eur. J. Clin. Microbiol. Infect. Dis. 2016, 35, 1227–1245. [Google Scholar] [CrossRef] [PubMed]
- Delahaye, F.; M’Hammedi, A.; Guerpillon, B.; De Gevigney, G.; Boibieux, A.; Dauwalder, O.; Bouchiat, C.; Vandenesch, F. Systematic Search for Present and Potential Portals of Entry for Infective Endocarditis. J. Am. Coll. Cardiol. 2016, 67, 151–158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Forner, L.; Larsen, T.; Kilian, M.; Holmstrup, P. Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J. Clin. Periodontol. 2006, 33, 401–407. [Google Scholar] [CrossRef] [PubMed]
- Almuhaideb, A.; Papathanasiou, N.; Bomanji, J. 18F-FDG PET/CT imaging in oncology. Ann. Saudi Med. 2011, 31, 3–13. [Google Scholar] [CrossRef] [Green Version]
- Mahmood, M.; Kendi, A.T.; Ajmal, S.; Farid, S.; O’Horo, J.C.; Chareonthaitawee, P.; Baddour, L.M.; Sohail, M.R. Meta-analysis of 18F-FDG PET/CT in the diagnosis of infective endocarditis. J. Nucl. Cardiol. 2017, 26, 922–935. [Google Scholar] [CrossRef]
- Heuker, M.; Sijbesma, J.W.A.; Suárez, R.A.; De Jong, J.R.; Boersma, H.H.; Luurtsema, G.; Elsinga, P.H.; Glaudemans, A.W.J.M.; Van Dam, G.M.; Van Dijl, J.M.; et al. In vitro imaging of bacteria using 18F-fluorodeoxyglucose micro positron emission tomography. Sci. Rep. 2017, 7, 4973. [Google Scholar] [CrossRef]
- Carvalho-Sousa, B.; Gomes, F.D.A.; Ferreira, C.M.; Rocha, M.M.D.N.P.; Barros, E.B.; De Albuquerque, D.S. Persistent extra-radicular bacterial biofilm in endodontically treated human teeth: Scanning electron microscopy analysis after apical surgery. Microsc. Res. Tech. 2017, 80, 662–667. [Google Scholar] [CrossRef]
- Irani, S. Orofacial Bacterial Infectious Diseases: An Update. J. Int. Soc. Prev. Community Dent. 2017, 7, S61–S67. [Google Scholar] [CrossRef]
- Yamashiro, K.; Nakano, M.; Sawaki, K.; Okazaki, F.; Hirata, Y.; Takashiba, S. The potential of positron emission tomography/computerized tomography (PET/CT) scanning as a detector of high-risk patients with oral infection during preoperative staging. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2016, 122, 242–249. [Google Scholar] [CrossRef]
- Benouaich, V.; Hitzel, A.; Armand, S. Relevance of functional imaging in dental implantology. J. Clin. Exp. Dent. 2018, 10, e1011–e1016. [Google Scholar] [CrossRef]
- Gomes, A.; Glaudemans, A.W.J.M.; Touw, D.J.; Van Melle, J.P.; Willems, T.P.; Maass, A.H.; Natour, E.; Prakken, N.H.J.; Borra, R.J.H.; Van Geel, P.P.; et al. Diagnostic value of imaging in infective endocarditis: A systematic review. Lancet Infect. Dis. 2017, 17, e1–e14. [Google Scholar] [CrossRef]
- Gomes, A.; van Geel, P.P.; Santing, M.; Prakken, N.H.J.; Ruis, M.L.; van Assen, S.; Slart, R.H.J.A.; Sinha, B.; Glaudemans, A.W.J.M. Imaging infective endocarditis: Adherence to a diagnostic flowchart and direct comparison of imaging techniques. J. Nucl. Cardiol. 2020, 27, 592–608. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Habib, G.; Lancellotti, P.; Antunes, M.J.; Bongiorni, M.G.; Casalta, J.P.; Del Zotti, F.; Dulgheru, R.; El Khoury, G.; Erba, P.A.; Iung, B.; et al. 2015 ESC Guidelines for the management of infective endocarditis: The task force for the management of infective endocarditis of the european society of cardiology (ESC). Endorsed by: European association for cardio-thoracic surgery (EACTS), the European Association of Nuclear Medicine (EANM). Eur. Heart J. 2015, 36, 3075–3128. [Google Scholar] [PubMed]
- Jamar, F.; Buscombe, J.; Chiti, A.; Christian, P.E.; Delbeke, D.; Donohoe, K.J.; Israel, O.; Martin-Comin, J.; Signore, A. EANM/SNMMI Guideline for 18F-FDG Use in Inflammation and Infection. J. Nucl. Med. 2013, 54, 647–658. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Erba, P.A.; Lancellotti, P.; Vilacosta, I.; Gaemperli, O.; Rouzet, F.; Hacker, M.; Signore, A.; Slart, R.H.J.A.; Habib, G. Recommendations on nuclear and multimodality imaging in IE and CIED infections. Eur. J. Nucl. Med. Mol. Imaging 2018, 45, 1795–1815. [Google Scholar] [CrossRef] [PubMed]
- Shimamoto, H.; Tatsumi, M.; Kakimoto, N.; Hamada, S.; Shimosegawa, E.; Murakami, S.; Furukawa, S.; Hatazawa, J. 18F-FDG accumulation in the oral cavity is associated with periodontal disease and apical periodontitis: An initial demonstration on PET/CT. Ann. Nucl. Med. 2008, 22, 587–593. [Google Scholar] [CrossRef]
- Kito, S.; Koga, H.; Kodama, M.; Yamamoto, N.; Kokuryo, S.; Habu, M.; Matsuo, K.; Nishino, T.; Kubota, K.; Muraoka, K.; et al. Reflection of 18F-FDG accumulation in the evaluation of the extent of periapical or periodontal inflammation. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2012, 114, e62–e69. [Google Scholar] [CrossRef]
- Kao, C.-H. Incidental Findings of FDG Uptake in Dental Caries. Clin. Nucl. Med. 2003, 28, 610. [Google Scholar] [CrossRef]
- Pasha, M.A.; Marcus, C.; Fakhry, C.; Kang, H.; Kiess, A.P.; Subramaniam, R.M. FDG PET/CT for Management and Assessing Outcomes of Squamous Cell Cancer of the Oral Cavity. Am. J. Roentgenol. 2015, 205, W150–W161. [Google Scholar] [CrossRef]
- Tubiana, S.; Blotière, P.-O.; Hoen, B.; Lesclous, P.; Millot, S.; Rudant, J.; Weill, A.; Coste, J.; Alla, F.; Duval, X. Dental procedures, antibiotic prophylaxis, and endocarditis among people with prosthetic heart valves: Nationwide population based cohort and a case crossover study. BMJ 2017, 358, j3776. [Google Scholar] [CrossRef] [Green Version]
- Cahill, T.J.; Harrison, J.L.; Jewell, P.; Onakpoya, I.; Chambers, J.B.; Dayer, M.; Lockhart, P.; Roberts, N.; Shanson, D.; Thornhill, M.; et al. Antibiotic prophylaxis for infective endocarditis: A systematic review and meta-analysis. Heart 2017, 103, 937–944. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wilson, W.; Taubert, K.A.; Gewitz, M.; Lockhart, P.B.; Baddour, L.M.; Levison, M.; Bolger, A.; Cabell, C.H.; Takahashi, M.; Baltimore, R.S.; et al. Prevention of infective endocarditis: Guidelines from the American heart sssociation. A guideline from the American heart association rheumatic fever, endocarditis and kawasaki disease committee, council on cardiovascular disease in the young, and the council on clinical cardiology, council on cardiovascular surgery and anesthesia, and the quality of care and outcomes research interdisciplinary working group. J. Am. Dent. Assoc. 2008, 139, 3–24. [Google Scholar]
- Rochlen, G.K.; Keenan, A.V. Value of prophylactic antibiotics for invasive dental procedures unclear. Evid. Based Dent. 2014, 15, 12–13. [Google Scholar] [CrossRef] [PubMed]
- Dayer, M.; Thornhill, M. Is antibiotic prophylaxis to prevent infective endocarditis worthwhile? J. Infect. Chemother. 2017, 13, 1–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thornhill, M.H.; Dayer, M.; Lockhart, P.B.; Prendergast, B. Antibiotic Prophylaxis of Infective Endocarditis. Curr. Infect. Dis. Rep. 2017, 19, 9. [Google Scholar] [CrossRef] [Green Version]
- Scottish Dental Clinical Effectiveness Programme. Drug Prescribing for Dentistry. Dental Clinical Guidance. Bacterial Infections. In Infective Endocarditis, 3rd ed.; Dundee Dental Education Centre: Dundee, UK, 2016; p. 29. [Google Scholar]
- Thornhill, M.; Dayer, M.J.; Forde, J.M.; Corey, G.R.; Chu, V.H.; Couper, D.; Lockhart, P.B. Impact of the NICE guideline recommending cessation of antibiotic prophylaxis for prevention of infective endocarditis: Before and after study. BMJ 2011, 342, d2392. [Google Scholar] [CrossRef] [Green Version]
- Dayer, M.J.; Jones, S.; Prendergast, B.; Baddour, L.M.; Lockhart, P.B.; Thornhill, M.H. Incidence of infective endocarditis in England, 2000–2013: A secular trend, interrupted time-series analysis. Lancet 2015, 385, 882–893. [Google Scholar] [CrossRef] [Green Version]
Group 1 (n = 19) | Group 2 (n = 14) | Group 3 (n = 19) | |
---|---|---|---|
Demographics | |||
Age (median (IQR), years) | 57 (42–66) | 60 (37–65) | 60 (51–70) |
Male sex, n (%) | 12 (63%) | 7 (50%) | 13 (68%) |
BMI (mean ±SD, kg/m2) | 25.1 ± 7.9 | 24.7 ± 2.7 | 25.5 ± 5.5 |
Diabetes, n (%) | 3 (16%) | 3 (21%) | 4 (21%) |
Previous IE, n (%) | 5 (26%) | 1 (7%) | 4 (21%) |
CIED, n (%) | 2 (11%) | 2 (14%) | 3 (16%) |
Previous PHV ○, n (%) | 16 (84%) | 7 (50%) | 6 (32%) |
Aortic | 10 (63%) | 6 (86%) | 5 (83%) |
Mitral | 1 (6%) | 1 (14%) | 1 (17%) |
Pulmonary | 4 (25%) | 0 | 0 |
Tricuspid | 1 (6%) | 0 | 0 |
Echocardiography data available ○, n (%) | 18 (95%) | 14 (100%) | 11 (58%) |
Vegetation ○○ | 12 (67%) | 1 (7%) | 0 |
Aortic | 6 (50%) | 0 | 0 |
Mitral | 3 (25%) | 0 | 0 |
Pulmonary | 1 (8%) | 1 (7%) | 0 |
Tricuspid | 2 (17%) | 0 | 0 |
Abscess | 2 (11%) | 1 (7%) | 0 |
Fistula | 0 | 0 | 0 |
Prosthetic valve dehiscence | 1 (6%) | 0 | 0 |
Paravalvular leakage | 6 (33%) | 1 (7%) | 0 |
CIED infection | 1 (6%) | 0 | 1 (10%) |
Microbiology data available ○○○, n (%) | 19 (100%) | 13 (93%) | 13 (68%) |
Positive blood cultures ○ | 12 (63%) | 8 (62%) | 6 (46%) |
Staphylococcus aureus | 4 (33%) | 6 (75%) | 4 (67%) |
Staphylococcus lugdunesis | 0 | 0 | 1 (17%) |
HACCEK ++ | 2 (17%) | 0 | 0 |
Streptococcus mitis | 3 (25%) | 0 | 0 |
Streptococcus bovis | 1 (8%) | 0 | 0 |
Streptococcus gallolyticus | 1 (8%) | 1 (13%) | 0 |
Streptococcus angiosus | 0 | 0 | 1 (17%) |
Other ## | 1 (8%) | 1 (13%) | 0 |
PCR and/or serology positive ○, n (%) | 5 (26%) | 0 | 0 |
Haemophilus parainfluenzae | 1 (5%) | 0 | 0 |
Tropheryma whipplei | 1 (5%) | 0 | 0 |
Enterobacter cloacae | 1 (5%) | 0 | 0 |
Escherichia coli | 1 (5%) | 0 | 0 |
Proprionibacterium acnes | 1 (5%) | 0 | 0 |
Valve culture, n (%) | 10 (53%) | 0 | 1 (5%) |
Staphylococcus aureus | 2 (20%) | 0 | 0 |
Haemophilus parainfluenzae | 1 (10%) | 0 | 0 |
Streptococcus mitis | 1 (10%) | 0 | 0 |
Proprionibacterium acnes | 1 (10%) | 0 | 1 (100%) |
No bacteria and yeast on the valve | 5 (50%) | 0 | 0 |
Lab test, n (%) | |||
CRP (median (IQR), mg/L) | 7.4 (2.8–46) | 89 (36.3–148.5) | 51 (19–145) |
Leucocytes (median (IQR), ×109/L | 8.2 (5.8–9.9) | 10.1 (7–13.8) | 9.6 (6.5-12) |
Treatment, n (%) | |||
Antibiotic therapy | 19 (100%) | 6 (43%) | 5 (26%) |
Days of antibiotic therapy (median (IQR)) ^^ | 14 (8–38) | 6 (6–9) | 6 (2–8) |
Valve surgery replacement | 13 (68%) | 0 | 2 (11%) |
Visual [18F]FDG Uptake Score ○ | |||||
---|---|---|---|---|---|
0 | 1 | 2 | 3 | Total | |
Dental Restorations | |||||
0 | 185 | 17 | 30 | 11 | 243 |
1 | 33 | 6 | 6 | 3 | 48 |
2 | 14 | 0 | 2 | 1 | 17 |
3 | 0 | 0 | 1 | 0 | 1 |
4 | 3 | 0 | 0 | 0 | 3 |
Total | 235 | 23 | 39 | 15 | 312 |
Root Canal Treatment | |||||
0 | 230 | 23 | 39 | 15 | 307 |
1 | 5 | 0 | 0 | 0 | 5 |
Total | 235 | 23 | 39 | 15 | 312 |
Extractions | |||||
0 | 219 | 23 | 37 | 15 | 294 |
1 | 7 | 0 | 2 | 0 | 9 |
2 | 3 | 0 | 0 | 0 | 3 |
4 | 4 | 0 | 0 | 0 | 4 |
6 | 2 | 0 | 0 | 0 | 2 |
Total | 235 | 23 | 39 | 15 | 312 |
Visual Score [18F]FDG Uptake (Mean ± SD) ○ | Oral SUVmax (Mean ± SD) | Extra-Cardiac Findings (MEAN ± SD) ○○ | Valve SUVmax (mean ± SD) ○○○ | |
---|---|---|---|---|
Group 1 | 0.51 ± 0.85 | 3.64 ± 2.18 | 1.95 ± 1.43 | 4.11 ± 1.84 |
Sextant 1 | 0.53 ± 0.84 | 3.24 ± 0.59 | ||
Sextant 2 | 0.47 ± 0.84 | 3.80 ± 2.09 | ||
Sextant 3 | 0.89 ± 1.05 | 4.17 ± 4.01 | ||
Sextant 4 | 0.32 ± 0.75 | 2.98 ± 1.29 | ||
Sextant 5 | 0.53 ± 0.77 | 3.97 ± 1.46 | ||
Sextant 6 | 0.32 ± 0.82 | 3.17 ± 1.77 | ||
Group 2 | 0.57 ± 1.01 | 3.65 ± 1.19 | 2.00 ± 1.47 | 3.04 ± 1.38 |
Sextant 1 | 0.43 ± 0.85 | 3.13 ± 0.70 | ||
Sextant 2 | 1.21 ± 1.31 | 4.50 ± 1.25 | ||
Sextant 3 | 0.50 ± 1.02 | 3.77 ± 0.51 | ||
Sextant 4 | 0.43 ± 0.85 | 3.05 ± 0.76 | ||
Sextant 5 | 0.50 ± 0.94 | 2.80 ± 1.74 | ||
Sextant 6 | 0.36 ± 0.93 | 4.70 ± 0.00 | ||
Group 3 | 0.35 ± 0.82 | 3.35 ± 1.08 | 2.84 ± 1.61 | 2.83 ± 0.54 |
Sextant 1 | 0.42 ± 0.90 | 3.40 ± 0.94 | ||
Sextant 2 | 0.32 ± 0.82 | 3.97 ± 1.21 | ||
Sextant 3 | 0.32 ± 0.82 | 2.80 ± 1.21 | ||
Sextant 4 | 0.74 ± 1.15 | 3.52 ± 1.38 | ||
Sextant 5 | 0.21 ± 0.54 | 3.28 ± 0.26 | ||
Sextant 6 | 0.11 ± 0.46 | 2.10 ± 0.00 |
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Dijkstra, G.W.; Glaudemans, A.W.J.M.; Erba, P.A.; Wouthuyzen-Bakker, M.; Sinha, B.; Vállez García, D.; van der Sluis, L.W.M.; Slart, R.H.J.A. Relationship between 18F-FDG Uptake in the Oral Cavity, Recent Dental Treatments, and Oral Inflammation or Infection: A Retrospective Study of Patients with Suspected Endocarditis. Diagnostics 2020, 10, 625. https://doi.org/10.3390/diagnostics10090625
Dijkstra GW, Glaudemans AWJM, Erba PA, Wouthuyzen-Bakker M, Sinha B, Vállez García D, van der Sluis LWM, Slart RHJA. Relationship between 18F-FDG Uptake in the Oral Cavity, Recent Dental Treatments, and Oral Inflammation or Infection: A Retrospective Study of Patients with Suspected Endocarditis. Diagnostics. 2020; 10(9):625. https://doi.org/10.3390/diagnostics10090625
Chicago/Turabian StyleDijkstra, Geertruida W., Andor W. J. M. Glaudemans, Paola A. Erba, Marjan Wouthuyzen-Bakker, Bhanu Sinha, David Vállez García, Luc W. M. van der Sluis, and Riemer H. J. A. Slart. 2020. "Relationship between 18F-FDG Uptake in the Oral Cavity, Recent Dental Treatments, and Oral Inflammation or Infection: A Retrospective Study of Patients with Suspected Endocarditis" Diagnostics 10, no. 9: 625. https://doi.org/10.3390/diagnostics10090625