Development of a new sonovue™ contrast-enhanced ultrasound approach reveals temporal and age-related features of muscle microvascular responses to feeding

Physiological Reports

Volumn 1, Issue 5, 2013, Pages

  Mitchell, William Kyle ^a,b   Phillips, Bethan E ^a   Williams, John P ^a,b   Rankin, Debbie ^a   Smith, Kenneth ^a   Lund, Jonathan N ^a,b   Atherton, Philip J ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b ROYAL DERBY HOSPITAL   (United Kingdom)

Author keywords

Aging; CEUS; Microcirculation; Muscle; Nutrition

Indexed keywords

ADULT; AGED; AGING; ARTICLE; BLOOD VESSEL REACTIVITY; BLOOD VOLUME; BODY MASS; CONTRAST-ENHANCED ULTRASOUND; DIET RESTRICTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; IMAGE SUBTRACTION; LEG BLOOD FLOW; LEG MUSCLE; MALE; MICROBUBBLE; MICROVASCULATURE; MUSCLE BLOOD FLOW; QUADRICEPS FEMORIS MUSCLE; SOUND INTENSITY; TEMPORALIS MUSCLE; ULTRASOUND TRANSDUCER; X RAY BONE DENSITOMETER; YOUNG ADULT;

EID: 85009062737     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.1002/phy2.119     Document Type: Article

References (57)

1. Amarteifio, E., M. A. Weber, S. Wormsbecher, S. Demirel, H. Krakowski-Roosen, A. Jores, et al. 2011. Dynamic contrast-enhanced ultrasound for assessment of skeletal muscle microcirculation in peripheral arterial disease. Invest. Radiol. 46: 504–508.
2. Atherton, P. J., T. Etheridge, P. W. Watt, D. Wilkinson, A. Selby, D. Rankin, et al. 2010. Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Am. J. Clin. Nutr. 92: 1080–1088.
3. Barrett-O’Keefe, Z., S. J. Ives, J. D. Trinity, G. Morgan, M. J. Rossman, A. J. Donato, et al. 2013a. Taming the “sleeping giant”: the role of endothelin-1 in the regulation of skeletal muscle blood flow and arterial blood pressure during exercise. Am. J. Physiol. Heart Circ. Physiol. 304: H162–H169.
4. Barrett-O’Keefe, Z., M. A. Witman, J. McDaniel, A. S. Fjeldstad, J. D. Trinity, S. J. Ives, et al. 2013b. Angiotensin II potentiates alpha-adrenergic vasoconstriction in the elderly. Clin. Sci. (Lond.) 124: 413–422.
5. Baumgartner, R. N., K. M. Koehler, D. Gallagher, L. Romero, S. B. Heymsfield, R. R. Ross, et al. 1998. Epidemiology of sarcopenia among the elderly in New Mexico. Am. J. Epidemiol. 147: 755–763.
6. Bloch, E. H., and A. S. Iberall. 1982. Toward a concept of the functional unit of mammalian skeletal muscle. Am. J. Physiol. 242: R411–R420.
7. Blomley, M., T. Albrecht, D. Cosgrove, V. Jayaram, J. Butler-Barnes, and R. Eckersley. 1998. Stimulated acoustic emission in liver parenchyma with Levovist. Lancet 351: 568.
8. Bohe, J., J. F. Low, R. R. Wolfe, and M. J. Rennie. 2001. Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. J. Physiol. 532: 575–579.
9. Celermajer, D. S., K. E. Sorensen, D. J. Spiegelhalter, D. Georgakopoulos, J. Robinson, and J. E. Deanfield. 1994. Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J. Am. Coll. Cardiol. 24: 471–476.
10. Clerk, L. H., M. A. Vincent, J. R. Lindner, M. G. Clark, S. Rattigan, and E. J. Barrett. 2004. The vasodilatory actions of insulin on resistance and terminal arterioles and their impact on muscle glucose uptake. Diabetes Metab. Res. Rev. 20: 3–12.
11. Coggan, A. R., R. J. Spina, D. S. King, M. A. Rogers, M. Brown, P. M. Nemeth, et al. 1992. Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. J. Gerontol. 47: B71–B76.
12. Cuthbertson, D., K. Smith, J. Babraj, G. Leese, T. Waddell, P. Atherton, et al. 2005. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 19: 422–424.
13. Dawson, D., M. A. Vincent, E. J. Barrett, S. Kaul, A. Clark, H. Leong-Poi, et al. 2002. Vascular recruitment in skeletal muscle during exercise and hyperinsulinemia assessed by contrast ultrasound. Am. J. Physiol. Endocrinol. Metab. 282: E714–E720.
14. Delashaw, J. B., and B. R. Duling. 1988. A study of the functional elements regulating capillary perfusion in striated muscle. Microvasc. Res. 36: 162–171.
15. Dinenno, F. A., P. P. Jones, D. R. Seals, and H. Tanaka. 1999. Limb blood flow and vascular conductance are reduced with age in healthy humans: relation to elevations in sympathetic nerve activity and declines in oxygen demand. Circulation 100: 164–170.
16. Donato, A. J., A. Uberoi, D. W. Wray, S. Nishiyama, L. Lawrenson, and R. S. Richardson. 2006. Differential effects of aging on limb blood flow in humans. Am. J. Physiol. Heart Circ. Physiol. 290: H272–H278.
17. Feletou, M. 2009. Calcium-activated potassium channels and endothelial dysfunction: therapeutic options? Br. J. Pharmacol. 156: 545–562.
18. Ferri, C., V. Pittoni, A. Piccoli, O. Laurenti, M. R. Cassone, C. Bellini, et al. 1995. Insulin stimulates endothelin-1 secretion from human endothelial cells and modulates its circulating levels in vivo. J. Clin. Endocrinol. Metab. 80: 829–835.
19. Frame, M. D., and I. H. Sarelius. 1993. Regulation of capillary perfusion by small arterioles is spatially organized. Circ. Res. 73: 155–163.
20. Goodwill, A. G., and J. C. Frisbee. 2012. Oxidant stress and skeletal muscle microvasculopathy in the metabolic syndrome. Vascul. Pharmacol. 57: 150–159.
21. Hayflick, L. 2007. Biological aging is no longer an unsolved problem. Ann. N. Y. Acad. Sci. 1100: 1–13.
22. Honig, C. R., C. L. Odoroff, and J. L. Frierson. 1980. Capillary recruitment in exercise: rate, extent, uniformity, and relation to blood flow. Am. J. Physiol. 238: H31–H42.
23. Honig, C. R., C. L. Odoroff, and J. L. Frierson. 1982. Active and passive capillary control in red muscle at rest and in exercise. Am. J. Physiol. 243: H196–H206.
24. Inoue, A., M. Yanagisawa, Y. Takuwa, Y. Mitsui, M. Kobayashi, and T. Masaki. 1989. The human preproendothelin-1 gene. Complete nucleotide sequence and regulation of expression. J. Biol. Chem. 264: 14954–14959.
25. Krix, M., F. Kiessling, N. Farhan, K. Schmidt, J. Hoffend, and S. Delorme. 2003. A multivessel model describing replenishment kinetics of ultrasound contrast agent for quantification of tissue perfusion. Ultrasound Med. Biol. 29: 1421–1430.
26. Krix, M., M. A. Weber, H. Krakowski-Roosen, H. B. Huttner, S. Delorme, H. U. Kauczor, et al. 2005. Assessment of skeletal muscle perfusion using contrast-enhanced ultrasonography. J. Ultrasound Med. 24: 431–441.
27. Krix, M., H. Krakowski-Roosen, H. U. Kauczor, S. Delorme, and M. A. Weber. 2009. Real-time contrast-enhanced ultrasound for the assessment of perfusion dynamics in skeletal muscle. Ultrasound Med. Biol. 35: 1587–1595.
28. Krix, M., M. A. Weber, H. U. Kauczor, S. Delorme, and H. Krakowski-Roosen. 2010. Changes in the micro-circulation of skeletal muscle due to varied isometric exercise assessed by contrast-enhanced ultrasound. Eur. J. Radiol. 76: 110–116.
29. Krogh, A. 1919. The supply of oxygen to the tissues and the regulation of the capillary circulation. J. Physiol. 52: 457–474.
30. Lind, L., and H. Lithell. 1993. Decreased peripheral blood flow in the pathogenesis of the metabolic syndrome comprising hypertension, hyperlipidemia, and hyperinsulinemia. Am. Heart J. 125: 1494–1497.
31. McGuire, J. J., H. Ding, and C. R. Triggle. 2001. Endothelium-derived relaxing factors: a focus on endothelium-derived hyperpolarizing factor (s). Can. J. Physiol. Pharmacol. 79: 443–470.
32. McKay, M. K., A. L. Gardner, D. Boyd, and R. L. Hester. 1998. Influence of venular prostaglandin release on arteriolar diameter during functional hyperemia. Hypertension 31: 213–217.
33. Mitchell, W. K., J. Williams, P. Atherton, M. Larvin, J. Lund, and M. Narici. 2012. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front. Physiol. 3: 260.
34. Morel, D. R., I. Schwieger, L. Hohn, J. Terrettaz, J. B. Llull, Y. A. Cornioley, et al. 2000. Human pharmacokinetics and safety evaluation of SonoVue, a new contrast agent for ultrasound imaging. Invest. Radiol. 35: 80–85.
35. Najjar, S. S., A. Scuteri, and E. G. Lakatta. 2005. Arterial aging: is it an immutable cardiovascular risk factor? Hypertension 46: 454–462.
36. Narici, M., and P. Cerretelli. 1998. Changes in human muscle architecture in disuse-atrophy evaluated by ultrasound imaging. J. Gravit. Physiol. 5: P73–P74.
37. Phillips, B., J. Williams, P. Atherton, K. Smith, W. Hildebrandt, D. Rankin, et al. 2012. Resistance exercise training improves age-related declines in leg vascular conductance and rejuvenates acute leg blood flow responses to feeding and exercise. J. Appl. Physiol. 112: 347–353.
38. Quaia, E. 2005. Contrast media in ultrasonography: basic principles and clinical applications. Springer, New York, NY.
39. Quaia, E., M. J. Blomley, S. Patel, C. J. Harvey, A. Padhani, P. Price, et al. 2002. Initial observations on the effect of irradiation on the liver-specific uptake of Levovist. Eur. J. Radiol. 41: 192–199.
40. Raitakari, O. T., N. Lai, K. Griffiths, R. McCredie, D. Sullivan, and D. S. Celermajer. 2000. Enhanced peripheral vasodilation in humans after a fatty meal. J. Am. Coll. Cardiol. 36: 417–422.
41. Rattigan, S., M. G. Clark, and E. J. Barrett. 1997. Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 46: 1381–1388.
42. Sarelius, I. H. 1993. Cell and oxygen flow in arterioles controlling capillary perfusion. Am. J. Physiol. 265: H1682–H1687.
43. Schneider, M., A. Broillet, I. Tardy, S. Pochon, P. Bussat, T. Bettinger, et al. 2012. Use of intravital microscopy to study the microvascular behavior of microbubble-based ultrasound contrast agents. Microcirculation 19: 245–259.
44. Seals, D. R., K. L. Moreau, P. E. Gates, and I. Eskurza. 2006. Modulatory influences on ageing of the vasculature in healthy humans. Exp. Gerontol. 41: 501–507.
45. Segal, S. S. 2005. Regulation of blood flow in the microcirculation. Microcirculation 12: 33–45.
46. Sjøberg, K. A., S. Rattigan, N. Hiscock, E. A. Richter, and B. Kiens. 2011. A new method to study changes in microvascular blood volume in muscle and adipose tissue: real-time imaging in humans and rat. Am. J. Physiol. Heart Circ. Physiol. 301: H450–H458.
47. Skilton, M. R., N. T. Lai, K. A. Griffiths, L. M. Molyneaux, D. K. Yue, D. R. Sullivan, et al. 2005. Meal-related increases in vascular reactivity are impaired in older and diabetic adults: insights into roles of aging and insulin in vascular flow. Am. J. Physiol. Heart Circ. Physiol. 288: H1404–H1410.
48. Steinberg, H. O., G. Brechtel, A. Johnson, N. Fineberg, and A. D. Baron. 1994. Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J. Clin. Investig. 94: 1172–1179.
49. Sweeney, T. E., and I. H. Sarelius. 1989. Arteriolar control of capillary cell flow in striated muscle. Circ. Res. 64: 112–120.
50. Tole, N. M. 2005. Ultrasound beam shape. Pp. 39–47 in H. Ostensen, ed. Basic physics of ultrasonic imaging. World Health Organisation, Geneva.
51. Vincent, M. A., D. Dawson, A. D. Clark, J. R. Lindner, S. Rattigan, M. G. Clark, et al. 2002. Skeletal muscle microvascular recruitment by physiological hyperinsulinemia precedes increases in total blood flow. Diabetes 51: 42–48.
52. Vincent, M. A., L. H. Clerk, J. R. Lindner, A. L. Klibanov, M. G. Clark, S. Rattigan, et al. 2004. Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 53: 1418–1423.
53. Wei, K., A. R. Jayaweera, S. Firoozan, A. Linka, D. M. Skyba, and S. Kaul. 1998. Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 97: 473–483.
54. Wilkes, E. A., A. L. Selby, P. J. Atherton, R. Patel, D. Rankin, K. Smith, et al. 2009. Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia. Am. J. Clin. Nutr. 90: 1343–1350.
55. Wolpert, H. A., S. N. Steen, N. W. Istfan, and D. C. Simonson. 1993. Insulin modulates circulating endothelin-1 levels in humans. Metabolism 42: 1027–1030.
56. Womack, L., D. Peters, E. J. Barrett, S. Kaul, W. Price, and J. R. Lindner. 2009. Abnormal skeletal muscle capillary recruitment during exercise in patients with type 2 diabetes mellitus and microvascular complications. J. Am. Coll. Cardiol. 53: 2175–2183.
57. Zhang, L., M. A. Vincent, S. M. Richards, L. H. Clerk, S. Rattigan, M. G. Clark, et al. 2004. Insulin sensitivity of muscle capillary recruitment in vivo. Diabetes 53: 447–453.