Diabetic foot syndrome: importance of calf muscles MR spectroscopy in the assessment of limb ischemia and effect of revascularization
Authors:
Andrea Němcová 1; Michal Dubský 1; Alexandra Jirkovská 1; Petr Šedivý 2; Miloslav Drobný 2; Milan Hájek 2; Monika Dezortová 2; Robert Bém 1; Vladimíra Fejfarová 1; Anna Pyšná 1
Authors‘ workplace:
Centrum diabetologie IKEM, Praha
1; Oddělení výpočetní tomografie, magnetické rezonance a klinické a experimentální spektroskopie Pracoviště radiodiagnostiky
a intervenční radiologie IKEM, Praha
2
Published in:
Vnitř Lék 2017; 63(4): 236-241
Category:
Original Contributions
Overview
Aim:
The standard method for assessment of effect of revascularization in patients with diabetic foot (DF) and critical limb ischemia (CLI) is transcutaneous oxygen pressure (TcPO2). Phosphorus magnetic resonance spectroscopy (31P MRS) enables to evaluate oxidative muscle metabolism that could be impaired in patients with diabetes and its complications. The aim of our study was to compare MRS of calf muscle between patients with DF and CLI and healthy controls and to evaluate the contribution of MRS in the assessment of the effect of revascularization.
Methods:
Thirty-four diabetic patients with DF and CLI treated either by autologous cell therapy (ACT; 15 patients) or percutaneous transluminal angioplasty (PTA; 12 patients) in our foot clinic during 2013–2016 and 19 healthy controls were included into the study. TcPO2 measurement was used as a standard method of non-invasive evaluation of limb ischemia. MRS examinations were performed using the whole-body 3T MR system 1 day before and 3 months after the procedure. Subjects were examined in a supine position with the coil fixed under the m. gastrocnemius. MRS parameters were obtained at rest and during the exercise period. Rest MRS parameters of oxidative muscle metabolism such as phosphocreatine (PCr), inorganic phosphate (Pi), phosphodiesters (PDE), adenosine triphosphate (ATP), dynamic MRS parameters such as recovery constant PCr (τPCr) and mitochondrial capacity (Qmax), and pH were compared between patients and healthy controls, and also before and 3 months after revascularization.
Results:
Patients with CLI had significantly lower PCr/Pi (p < 0.001), significantly higher Pi and pH (both p < 0.01), significantly lower Qmax and prolonged τPCr (both p < 0.001) in comparison with healthy controls. We observed a significant improvement in TcPO2 at 3 months after revascularization (from 26.4 ± 11.7 to 39.7 ± 17.7 mm Hg, p < 0.005). However, the rest MRS parameters did not change significantly after revascularization. In individual cases we observed improvement of dynamic MRS parameters. There was no correlation between MRS parameters and TcPO2 values.
Conclusion:
Results of our study show impaired oxidative metabolism of calf muscles in patients with CLI in comparison with healthy controls. We observed an improvement in dynamic MRS parameters in individual cases; this finding should be verified in a large number of patients during longer follow-up.
Key words:
autologous cell therapy – critical limb ischemia – diabetic foot – MR spectroscopy
Sources
1. Hinchliffe RJ, Brownrigg JR, Apelqvist J et al. IWGDF guidance on the diagnosis, prognosis and management of peripheral artery disease in patients with foot ulcers in diabetes. Diabetes Metab Res Rev 2016; 32(Suppl 1): 37–44. Dostupné z DOI: <http://dx.doi.org/10.1002/dmrr.2698>.
2. Dua A, Desai SS, Kumar N et al. Epidemiology and treatment strategies of iliac vein thrombophlebitis. Vascular 2015; 23(6): 599–601. Dostupné z DOI: <http://dx.doi.org/10.1177/1708538114565693>.
3. Brownrigg JR, Schaper NC, Hinchliffe RJ. Diagnosis and assessment of peripheral arterial disease in the diabetic foot. Diabet Med 2015; 32(6): 738–747. Dostupné z DOI: <http://dx.doi.org/10.1111/dme.12749>.
4. Benitez E, Sumpio BJ, Chin J et al. Contemporary assessment of foot perfusion in patients with critical limb ischemia. Semin Vasc Surg 2014; 27(1): 3–15. Dostupné z DOI: <http://dx.doi.org/10.1053/j.semvascsurg.2014.12.001>.
5. Liu Y, Xu Y, Fang F et al. Therapeutic Efficacy of Stem Cell-based Therapy in Peripheral Arterial Disease: A Meta-Analysis. PLoS One 2015; 10(4): e0125032. Dostupné z DOI: <http://dx.doi.org/10.1371/journal.pone.0125032>.
6. Tomesova J, Gruberova J, Broz P et al. Methods of skin microcirculation assessment. Vnitř Lék 2013; 59(10): 895–902.
7. Prompers JJ, Jeneson JA, Drost MR et al. Dynamic MRS and MRI of skeletal muscle function and biomechanics. NMR Biomed 2006; 19(7): 927–953.
8. Isbell DC, Berr SS, Toledano AY et al. Delayed calf muscle phosphocreatine recovery after exercise identifies peripheral arterial disease. J Am Coll Cardiol 2006; 47(11): 2289–2295.
9. Greiner A, Esterhammer R, Messner H et al. High-energy phosphate metabolism during incremental calf exercise in patients with unilaterally symptomatic peripheral arterial disease measured by phosphor 31 magnetic resonance spectroscopy. J Vasc Surg 2006; 43(5): 978–986.
10. Cree-Green M, Newcomer BR, Brown MS et al. Delayed skeletal muscle mitochondrial ADP recovery in youth with type 1 diabetes relates to muscle insulin resistance. Diabetes 2015; 64(2): 383–392. Dostupné z DOI: <http://dx.doi.org/10.2337/db14–0765>.
11. Petersen KF, Dufour S, Befroy D et al. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 2004; 350(7): 664–671.
12. Fetterman JL, Holbrook M, Westbrook DG et al. Mitochondrial DNA damage and vascular function in patients with diabetes mellitus and atherosclerotic cardiovascular disease. Cardiovasc Diabetol 2016; 15: 53. Dostupné z DOI: <http://dx.doi.org/10.1186/s12933–016–0372-y>.
13. Norgren L, Hiatt WR, Dormandy JA et al. Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II). Eur J Vasc Endovasc Surg 2007; 33(Suppl 1): S1-S75.
14. Graziani L, Silvestro A, Bertone V et al. Vascular involvement in diabetic subjects with ischemic foot ulcer: a new morphologic categorization of disease severity. Eur J Vasc Endovasc Surg 2007; 33(4): 453–460.
15. Dubsky M, Jirkovska A, Bem R et al. Comparison of the effect of stem cell therapy and percutaneous transluminal angioplasty on diabetic foot disease in patients with critical limb ischemia. Cytotherapy 2014; 16(12): 1733–1738. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jcyt.2014.08.010>.
16. Sedivy P, Kipfelsberger MC, Dezortova M et al. Dynamic 31P MR spectroscopy of plantar flexion: influence of ergometer design, magnetic field strength (3 and 7 T), and RF-coil design. Med Phys 2015; 42(4): 1678–1689. Dostupné z DOI: <http://dx.doi.org/10.1118/1.4914448>.
17. Torriani M, Townsend E, Thomas BJ et al. Lower leg muscle involvement in Duchenne muscular dystrophy: an MR imaging and spectroscopy study. Skeletal Radiol 2012; 41(4): 437–445. Dostupné z DOI: <http://dx.doi.org/10.1007/s00256–011–1240–1>.
18. D‘Souza DM, Al-Sajee D, Hawke TJ. Diabetic myopathy: impact of diabetes mellitus on skeletal muscle progenitor cells. Front Physiol 2013; 4: 379. Dostupné z DOI: <http://dx.doi.org/10.3389/fphys.2013.00379>.
19. Brass EP, Hiatt WR. Acquired skeletal muscle metabolic myopathy in atherosclerotic peripheral arterial disease. Vasc Med 2000; 5(1): 55–59.
20. Pipinos II, Judge AR, Selsby JT et al. The myopathy of peripheral arterial occlusive disease: part 1. Functional and histomorphological changes and evidence for mitochondrial dysfunction. Vasc Endovascular Surg 2007; 41(6): 481–489. Dostupné z DOI: <http://dx.doi.org/10.1177/1538574407311106>.
21. Greiner A, Esterhammer R, Bammer D et al. High-energy phosphate metabolism in the calf muscle of healthy humans during incremental calf exercise with and without moderate cuff stenosis. Eur J Appl Physiol 2007; 99(5): 519–531.
22. Schocke MF, Esterhammer R, Kammerlander C et al. High-energy phosphate metabolism during incremental calf exercise in humans measured by 31 phosphorus magnetic resonance spectroscopy (31P MRS). Magn Reson Imaging 2004; 22(1): 109–115.
23. Tecilazich F, Dinh T, Lyons TE et al. Postexercise phosphocreatine recovery, an index of mitochondrial oxidative phosphorylation, is reduced in diabetic patients with lower extremity complications. J Vasc Surg 2013; 57(4): 997–1005. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jvs.2012.10.011>.
24. West AM, Anderson JD, Epstein FH et al. Percutaneous intervention in peripheral artery disease improves calf muscle phosphocreatine recovery kinetics: a pilot study. Vasc Med 2012; 17(1): 3–9. Dostupné z DOI: <http://dx.doi.org/10.1177/1358863X11431837>.
25. Jirkovska A. Diabetic foot syndrome from the perspective of internist educated in podiatry. Vnitř Lék 2016; 62(Suppl 4): 42–47.
26. Jubrias SA, Crowther GJ, Shankland EG et al. Acidosis inhibits oxidative phosphorylation in contracting human skeletal muscle in vivo. J Physiol 2003; 553(Pt 2): 589–599.
Labels
Diabetology Endocrinology Internal medicineArticle was published in
Internal Medicine
2017 Issue 4
Most read in this issue
- Relapsing autoimmune pancreatitis type 1: case report
- Controversies around QALYs
- AT1 blockers – comparability with ACE inhibitors
- Novelties in the treatment of heart failure