Yeungnam Univ J Med.  2021 Apr;38(2):95-106. 10.12701/yujm.2020.00479.

F-18 fluorodeoxyglucose positron emission tomography/computed tomography in the infection of heart

• Kong E

• KMID: 2515183
• DOI: http://doi.org/10.12701/yujm.2020.00479

Abstract

Infections involving the heart are becoming increasingly common, and a timely diagnosis of utmost importance, despite its challenges. F-18 fluorodeoxyglucose (FDG) positron emission tomography/computed tomography (PET/CT) is a recently introduced diagnostic tool in cardiology. This review focuses on the current evidence for the use of FDG PET/CT in the diagnosis of infective endocarditis, cardiac implantable device infection, left ventricular assist device infection, and secondary complications. The author discusses considerations when using FDG PET/CT in routine clinical practice, patient preparation for reducing physiologic myocardial uptake, acquisition of images, and interpretation of PET/CT findings. This review also functions to highlight the need for a standardized acquisition protocol.

Keyword

Endocarditis; Fluorodeoxyglucose F18; Infections; Positron emission tomography computed tomography; Heart valve prosthesis

Figure

• 

  Fig. 1. Two patients (A–D and E–H) with suspected cardiac implantable electronic device (CIED) infection. (A) Gross photo showing CIED exposure with redness in a 79-year-old woman. (B) Echocardiography reveals vegetation in the mitral valve. (C, D) Axial FDG PET/CT shows no FDG uptake in the CIED pocket, but shows high uptake in the mitral valve. The patient did not undergo extraction of the CIED, and instead, was treated with vancomycin for CIED-infective endocarditis with positive blood culture for Staphylococcus epidermidis. (E) Gross photo showing pus drainage from the pacemaker insertion site in a 73-year-old man with positive wound culture for Serratia marcescens. (F) Echocardiography confirming absence of abnormal findings in the heart. (G, H) Axial and coronal FDG PET/CT shows increased FDG uptake in the pocket and along the lead. The patient underwent pacemaker removal. FDG, F-18 fluorodeoxyglucose; PET/CT, positron emission tomography/computed tomography.

• 

  Fig. 2. (A) Extracardiac metastatic infection in a 51-year-old woman demonstrating bilateral lung infection and spondylodiscitis resulting from Staphylococcus aureus. (B) Axial FDG PET, (C) axial FDG PET/CT, and (D) axial lung CT showing extensive lung septic emboli. (E) Sagittal FDG PET/CT, (F) sagittal FDG PET, and (G) coronal FDG PET/CT showing infective spondylodiscitis in T10 to T11. FDG, F-18 fluorodeoxyglucose; PET, positron emission tomography; CT, computed tomography.

• 

  Fig. 3. (A) Axial FDG ETP/CT, (B) non-attenuation, and (C) AC PET images of a case of definite infective endocarditis (IE) resulting from Escherichia coli in an 89-year-old patient with a mitral native valve. She suffered from fever of unknown origin, and FDG PET/CT was performed to evaluate the source of the fever. FDG PET/CT shows focal areas of enhanced glycolytic metabolism (arrow) around the calcified mitral valve, in which the standard uptake value was 5.8. Dense calcification can result in false uptake through AC, and therefore, readers should check for non-AC PET. FDG, F-18 fluorodeoxyglucose; PET, positron emission tomography; CT, computed tomography.

Reference

References

1. Sunil M, Hieu HQ, Arjan Singh RS, Ponnampalavanar S, Siew KS, Loch A. Evolving trends in infective endocarditis in a developing country: a consequence of medical progress? Ann Clin Microbiol Antimicrob. 2019; 18:43.

2. Murillo H, Restrepo CS, Marmol-Velez JA, Vargas D, Ocazionez D, Martinez-Jimenez S, et al. Infectious diseases of the heart: pathophysiology, clinical and imaging overview. Radiographics. 2016; 36:963–83.

3. Johansen JB, Jørgensen OD, Møller M, Arnsbo P, Mortensen PT, Nielsen JC. Infection after pacemaker implantation: infection rates and risk factors associated with infection in a population-based cohort study of 46299 consecutive patients. Eur Heart J. 2011; 32:991–8.

4. Li JS, Sexton DJ, Mick N, Nettles R, Fowler VG Jr, Ryan T, et al. Proposed modifications to the Duke criteria for the diagnosis of infective endocarditis. Clin Infect Dis. 2000; 30:633–8.

5. Habib G, Lancellotti P, Antunes MJ, Bongiorni MG, Casalta JP, Del Zotti F, 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; 36:3075–128.

6. Pizzi MN, Roque A, Fernández-Hidalgo N, Cuéllar-Calabria H, Ferreira-González I, Gonzàlez-Alujas MT, et al. Improving the diagnosis of infective endocarditis in prosthetic valves and intracardiac devices with 18F-fluordeoxyglucose positron emission tomography/computed tomography angiography: initial results at an infective endocarditis referral center. Circulation. 2015; 132:1113–26.

7. Saby L, Laas O, Habib G, Cammilleri S, Mancini J, Tessonnier L, et al. Positron emission tomography/computed tomography for diagnosis of prosthetic valve endocarditis: increased valvular 18F-fluorodeoxyglucose uptake as a novel major criterion. J Am Coll Cardiol. 2013; 61:2374–82.

8. Dilsizian V, Achenbach S, Narula J. Adding or selecting imaging modalities for incremental diagnosis: a case study of 18FDG PET/CT in prosthetic valve endocarditis. JACC Cardiovasc Imaging. 2013; 6:1020–1.

9. Dilsizian V, Bacharach SL, Beanlands RS, Bergmann SR, Delbeke D, Dorbala S, et al. ASNC imaging guidelines/SNMMI procedure standard for positron emission tomography (PET) nuclear cardiology procedures. J Nucl Cardiol. 2016; 23:1187–226.

10. Chen W, Sajadi MM, Dilsizian V. Merits of FDG PET/CT and functional molecular imaging over anatomic imaging with echocardiography and CT angiography for the diagnosis of cardiac device infections. JACC Cardiovasc Imaging. 2018; 11:1679–91.

11. Doherty JU, Kort S, Mehran R, Schoenhagen P, Soman P. ACC/AATS/AHA/ASE/ASNC/HRS/SCAI/SCCT/SCMR/STS 2017 appropriate use criteria for multimodality imaging in valvular heart disease: a report of the American College of Cardiology Appropriate Use Criteria Task Force, American Association for Thoracic Surgery, American Heart Association, American Society of Echocardiography, American Society of Nuclear Cardiology, Heart Rhythm Society, Society for Cardiovascular Angiography and Interventions, Society of Cardiovascular Computed Tomography, Society for Cardiovascular Magnetic Resonance, and Society of Thoracic Surgeons. J Am Coll Cardiol. 2017; 70:1647–72.

12. Baddour LM, Wilson WR, Bayer AS, Fowler VG Jr, Tleyjeh IM, Rybak MJ, et al. Infective endocarditis in adults: diagnosis, antimicrobial therapy, and management of complications: a scientific statement for healthcare professionals from the American Heart Association. Circulation. 2015; 132:1435–86.

13. Mahmood M, Kendi AT, Ajmal S, Farid S, O’Horo JC, Chareonthaitawee P, et al. Meta-analysis of 18F-FDG PET/CT in the diagnosis of infective endocarditis. J Nucl Cardiol. 2019; 26:922–35.

14. Swart LE, Gomes A, Scholtens AM, Sinha B, Tanis W, Lam MG, et al. Improving the diagnostic performance of 18F-fluorodeoxyglucose positron-emission tomography/computed tomography in prosthetic heart valve endocarditis. Circulation. 2018; 138:1412–27.

15. de Camargo RA, Sommer Bitencourt M, Meneghetti JC, Soares J, Gonçalves LF, Buchpiguel CA, et al. The role of 18F-fluorodeoxyglucose positron emission tomography/computed tomography in the diagnosis of left-sided endocarditis: native vs prosthetic valves endocarditis. Clin Infect Dis. 2020; 70:583–94.

16. San S, Ravis E, Tessonier L, Philip M, Cammilleri S, Lavagna F, et al. Prognostic value of 18F-fluorodeoxyglucose positron emission tomography/computed tomography in infective endocarditis. J Am Coll Cardiol. 2019; 74:1031–40.

17. Kouijzer IJ, Berrevoets MA, Aarntzen EH, de Vries J, van Dijk AP, Oyen WJ, et al. 18F-fluorodeoxyglucose positron-emission tomography combined with computed tomography as a diagnostic tool in native valve endocarditis. Nucl Med Commun. 2018; 39:747–52.

18. Kestler M, Muñoz P, Rodríguez-Créixems M, Rotger A, Jimenez-Requena F, Mari A, et al. Role of (18)F-FDG PET in patients with infectious endocarditis. J Nucl Med. 2014; 55:1093–8.

19. Kusumoto FM, Schoenfeld MH, Wilkoff BL, Berul CI, Birgersdotter-Green UM, Carrillo R, et al. 2017 HRS expert consensus statement on cardiovascular implantable electronic device lead management and extraction. Heart Rhythm. 2017; 14:e503–51.

20. Athan E, Chu VH, Tattevin P, Selton-Suty C, Jones P, Naber C, et al. Clinical characteristics and outcome of infective endocarditis involving implantable cardiac devices. JAMA. 2012; 307:1727–35.

21. Podoleanu C, Deharo JC. Management of cardiac implantable electronic device infection. Arrhythm Electrophysiol Rev. 2014; 3:184–9.

22. Sarrazin JF, Philippon F, Tessier M, Guimond J, Molin F, Champagne J, et al. Usefulness of fluorine-18 positron emission tomography/computed tomography for identification of cardiovascular implantable electronic device infections. J Am Coll Cardiol. 2012; 59:1616–25.

23. Juneau D, Golfam M, Hazra S, Zuckier LS, Garas S, Redpath C, et al. Positron emission tomography and single-photon emission computed tomography imaging in the diagnosis of cardiac implantable electronic device infection: a systematic review and meta-analysis. Circ Cardiovasc Imaging. 2017; 10:e005772.

24. Mahmood M, Kendi AT, Farid S, Ajmal S, Johnson GB, Baddour LM, et al. Role of 18F-FDG PET/CT in the diagnosis of cardiovascular implantable electronic device infections: a meta-analysis. J Nucl Cardiol. 2019; 26:958–70.

25. Jiménez-Ballvé A, Pérez-Castejón MJ, Delgado-Bolton RC, Sánchez-Enrique C, Vilacosta I, Vivas D, et al. Assessment of the diagnostic accuracy of 18F-FDG PET/CT in prosthetic infective endocarditis and cardiac implantable electronic device infection: comparison of different interpretation criteria. Eur J Nucl Med Mol Imaging. 2016; 43:2401–12.

26. Diemberger I, Bonfiglioli R, Martignani C, Graziosi M, Biffi M, Lorenzetti S, et al. Contribution of PET imaging to mortality risk stratification in candidates to lead extraction for pacemaker or defibrillator infection: a prospective single center study. Eur J Nucl Med Mol Imaging. 2019; 46:194–205.

27. Kadakia S, Moore R, Ambur V, Toyoda Y. Current status of the implantable LVAD. Gen Thorac Cardiovasc Surg. 2016; 64:501–8.

28. Koval CE, Thuita L, Moazami N, Blackstone E. Evolution and impact of drive-line infection in a large cohort of continuous-flow ventricular assist device recipients. J Heart Lung Transplant. 2014; 33:1164–72.

29. Bernhardt AM, Pamirsad MA, Brand C, Reichart D, Tienken M, Barten MJ, et al. The value of fluorine-18 deoxyglucose positron emission tomography scans in patients with ventricular assist device specific infections. Eur J Cardiothorac Surg. 2017; 51:1072–7.

30. Tam MC, Patel VN, Weinberg RL, Hulten EA, Aaronson KD, Pagani FD, et al. Diagnostic accuracy of FDG PET/CT in suspected LVAD infections: a case series, systematic review, and meta-analysis. JACC Cardiovasc Imaging. 2020; 13:1191–202.

31. Akin S, Muslem R, Constantinescu AA, Manintveld OC, Birim O, Brugts JJ, et al. 18F-FDG PET/CT in the diagnosis and management of continuous flow left ventricular assist device infections: a case series and review of the literature. ASAIO J. 2018; 64:e11–9.

32. Kim J, Feller ED, Chen W, Liang Y, Dilsizian V. FDG PET/CT for early detection and localization of left ventricular assist device infection: impact on patient management and outcome. JACC Cardiovasc Imaging. 2019; 12:722–9.

33. de Vaugelade C, Mesguich C, Nubret K, Camou F, Greib C, Dournes G, et al. Infections in patients using ventricular-assist devices: comparison of the diagnostic performance of 18F-FDG PET/CT scan and leucocyte-labeled scintigraphy. J Nucl Cardiol. 2019; 26:42–55.

34. Sommerlath Sohns JM, Kröhn H, Schöde A, Derlin T, Haverich A, Schmitto JD, et al. 18F-FDG PET/CT in left-ventricular assist device infection: initial results supporting the usefulness of image-guided therapy. J Nucl Med. 2020; 61:971–6.

35. Kanapinn P, Burchert W, Körperich H, Körfer J. 18F-FDG PET/CT-imaging of left ventricular assist device infection: a retrospective quantitative intrapatient analysis. J Nucl Cardiol. 2019; 26:1212–21.

36. Dell’Aquila AM, Avramovic N, Mastrobuoni S, Motekallemi A, Wisniewski K, Scherer M, et al. Fluorine-18 fluorodeoxyglucose positron emission tomography/computed tomography for improving diagnosis of infection in patients on CF-LVAD: longing for more ‘insights’. Eur Heart J Cardiovasc Imaging. 2018; 19:532–43.

37. Avramovic N, Dell’Aquila AM, Weckesser M, Milankovic D, Vrachimis A, Sindermann JR, et al. Metabolic volume performs better than SUVmax in the detection of left ventricular assist device driveline infection. Eur J Nucl Med Mol Imaging. 2017; 44:1870–7.

38. Van Riet J, Hill EE, Gheysens O, Dymarkowski S, Herregods MC, Herijgers P, et al. (18)F-FDG PET/CT for early detection of embolism and metastatic infection in patients with infective endocarditis. Eur J Nucl Med Mol Imaging. 2010; 37:1189–97.

39. Mikail N, Benali K, Mahida B, Vigne J, Hyafil F, Rouzet F, et al. 18F-FDG-PET/CT imaging to diagnose septic emboli and mycotic aneurysms in patients with endocarditis and cardiac device infections. Curr Cardiol Rep. 2018; 20:14.

40. Orvin K, Goldberg E, Bernstine H, Groshar D, Sagie A, Kornowski R, et al. The role of FDG-PET/CT imaging in early detection of extra-cardiac complications of infective endocarditis. Clin Microbiol Infect. 2015; 21:69–76.

41. Nishimura RA, Otto CM, Bonow RO, Carabello BA, Erwin JP 3rd, Guyton RA, et al. 2014 AHA/ACC guideline for the management of patients with valvular heart disease: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2014; 63:2438–88.

42. Wintenberger C, Guery B, Bonnet E, Castan B, Cohen R, Diamantis S, et al. Proposal for shorter antibiotic therapies. Med Mal Infect. 2017; 47:92–141.

43. Puerta-Alcalde P, Cuervo G, Simonetti AF, Gracia-Sánchez L, Ortiz D, Garcia-Vidal C. PET/CT added to Duke criteria facilitates diagnosis and monitoring of long-term suppressive therapy of prosthetic endocarditis. Infect Dis (Lond). 2017; 49:698–701.

44. García JR, Fortuny C, Riaza L, Soler M, Bassa P, Riera E. Diagnosis by (18)F-FDG PET/CT of infective endocarditis, staging and monitoring of antibiotic treatment after transposition of surgically corrected great arteries. Rev Esp Med Nucl Imagen Mol. 2016; 35:115–7.

45. Aguadé Bruix S, Roque Pérez A, Cuéllar Calabria H, Pizzi MN. Cardiac 18F-FDG PET/CT procedure for the diagnosis of prosthetic endocarditis and intracardiac devices. Rev Esp Med Nucl Imagen Mol. 2018; 37:163–71.

46. Scholtens AM, Swart LE, Verberne HJ, Tanis W, Lam MG, Budde RP. Confounders in FDG-PET/CT imaging of suspected prosthetic valve endocarditis. JACC Cardiovasc Imaging. 2016; 9:1462–5.

47. Yoshinaga K, Tamaki N. Imaging myocardial metabolism. Curr Opin Biotechnol. 2007; 18:52–9.

48. Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose fatty-acid cycle: its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet. 1963; 1:785–9.

49. Mochizuki T, Tsukamoto E, Kuge Y, Kanegae K, Zhao S, Hikosaka K, et al. FDG uptake and glucose transporter subtype expressions in experimental tumor and inflammation models. J Nucl Med. 2001; 42:1551–5.

50. Depre C, Vanoverschelde JL, Taegtmeyer H. Glucose for the heart. Circulation. 1999; 99:578–88.

51. Osborne MT, Hulten EA, Murthy VL, Skali H, Taqueti VR, Dorbala S, et al. Patient preparation for cardiac fluorine-18 fluorodeoxyglucose positron emission tomography imaging of inflammation. J Nucl Cardiol. 2017; 24:86–99.

52. Dorbala S, Di Carli MF, Delbeke D, Abbara S, DePuey EG, Dilsizian V, et al. SNMMI/ASNC/SCCT guideline for cardiac SPECT/CT and PET/CT 1.0. J Nucl Med. 2013; 54:1485–507.

53. Kumita S, Yoshinaga K, Miyagawa M, Momose M, Kiso K, Kasai T, et al. Recommendations for 18F-fluorodeoxyglucose positron emission tomography imaging for diagnosis of cardiac sarcoidosis-2018 update: Japanese Society of Nuclear Cardiology recommendations. J Nucl Cardiol. 2019; 26:1414–33.

54. Asmal AC, Leary WP, Thandroyen F, Botha J, Wattrus S. A dose-response study of the anticoagulant and lipolytic activities of heparin in normal subjects. Br J Clin Pharmacol. 1979; 7:531–3.

55. Persson E, Nordenström J, Nilsson-Ehle P, Hagenfeldt L, Wahren J. Plasma lipolytic activity and substrate oxidation after intravenous administration of heparin and a low molecular weight heparin fragment. Clin Physiol. 1990; 10:573–83.

56. Scholtens AM, Verberne HJ, Budde RP, Lam MG. Additional heparin preadministration improves cardiac glucose metabolism suppression over low-carbohydrate diet alone in 18F-FDG PET imaging. J Nucl Med. 2016; 57:568–73.

57. Gaeta C, Fernández Y, Pavía J, Flotats A, Artigas C, Deportos J, et al. Reduced myocardial 18F-FDG uptake after calcium channel blocker administration. Initial observation for a potential new method to improve plaque detection. Eur J Nucl Med Mol Imaging. 2011; 38:2018–24.

58. Demeure F, Hanin FX, Bol A, Vincent MF, Pouleur AC, Gerber B, et al. A randomized trial on the optimization of 18F-FDG myocardial uptake suppression: implications for vulnerable coronary plaque imaging. J Nucl Med. 2014; 55:1629–35.

59. Caldarella C, Leccisotti L, Treglia G, Giordano A. Which is the optimal acquisition time for FDG PET/CT imaging in patients with infective endocarditis? J Nucl Cardiol. 2013; 20:307–9.

60. Scholtens AM, Swart LE, Verberne HJ, Budde RP, Lam MG. Dual-time-point FDG PET/CT imaging in prosthetic heart valve endocarditis. J Nucl Cardiol. 2018; 25:1960–7.

61. Asmar A, Ozcan C, Diederichsen AC, Thomassen A, Gill S. Clinical impact of 18F-FDG-PET/CT in the extra cardiac work-up of patients with infective endocarditis. Eur Heart J Cardiovasc Imaging. 2014; 15:1013–9.

62. Slomka PJ, Nishina H, Berman DS, Kang X, Akincioglu C, Friedman JD, et al. “Motion-frozen” display and quantification of myocardial perfusion. J Nucl Med. 2004; 45:1128–34.

63. Pizzi MN, Dos-Subirà L, Roque A, Fernández-Hidalgo N, Cuéllar-Calabria H, Pijuan Domènech A, et al. 18F-FDG-PET/CT angiography in the diagnosis of infective endocarditis and cardiac device infection in adult patients with congenital heart disease and prosthetic material. Int J Cardiol. 2017; 248:396–402.

64. Balmforth D, Chacko J, Uppal R. Does positron emission tomography/computed tomography aid the diagnosis of prosthetic valve infective endocarditis? Interact Cardiovasc Thorac Surg. 2016; 23:648–52.

65. Mathieu C, Mikaïl N, Benali K, Iung B, Duval X, Nataf P, et al. Characterization of 18F-fluorodeoxyglucose uptake pattern in noninfected prosthetic heart valves. Circ Cardiovasc Imaging. 2017; 10:e005585.

66. Scholtens AM, Budde RP, Lam MG, Verberne HJ. FDG PET/CT in prosthetic heart valve endocarditis: there is no need to wait. J Nucl Cardiol. 2017; 24:1540–1.

67. Abikhzer G, Martineau P, Grégoire J, Finnerty V, Harel F, Pelletier-Galarneau M. [18F]FDG-PET CT for the evaluation of native valve endocarditis. J Nucl Cardiol. 2020; Mar. 16. [Epub]. http://doi.org/10.1007/s12350-020-02092-6.

68. Ahmed FZ, James J, Tout D, Arumugam P, Mamas M, Zaidi AM. Metal artefact reduction algorithms prevent false positive results when assessing patients for cardiac implantable electronic device infection. J Nucl Cardiol. 2015; 22:219–20.

69. Scholtens AM, Verberne HJ. Attenuation correction and metal artifact reduction in FDG PET/CT for prosthetic heart valve and cardiac implantable device endocarditis. J Nucl Cardiol. 2018; 25:2172–3.

70. Scholtens AM, Swart LE, Kolste HJ, Budde RP, Lam MG, Verberne HJ. Standardized uptake values in FDG PET/CT for prosthetic heart valve endocarditis: a call for standardization. J Nucl Cardiol. 2018; 25:2084–91.

71. Hyafil F, Rouzet F, Le Guludec D. Quantification of FDG uptake in patients with a suspicion of prosthetic valve endocarditis: part of the problem or part of the solution? J Nucl Cardiol. 2018; 25:2092–5.

72. Rousset O, Rahmim A, Alavi A, Zaidi H. Partial volume correction strategies in PET. PET Clin. 2007; 2:235–49.

73. Salavati A, Borofsky S, Boon-Keng TK, Houshmand S, Khiewvan B, Saboury B, et al. Application of partial volume effect correction and 4D PET in the quantification of FDG avid lung lesions. Mol Imaging Biol. 2015; 17:140–8.