Exercise training improves cutaneous microvascular function in nonalcoholic fatty liver disease

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 1, 2013, Pages

  Pugh, Christopher J A ^a,d   Cuthbertson, Daniel J ^b   Sprung, Victoria S ^a   Kemp, Graham J ^b   Richardson, Paul ^c   Margot Umpleby, A ^e   Green, Daniel J ^a,d   Timothy Cable, N ^a   Jones, Helen ^a  

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c ROYAL LIVERPOOL UNIVERSITY HOSPITAL   (United Kingdom)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Cutaneous microvessel function; Exercise; Exercise training; Microvascular function; Nitric oxide; Nonalcoholic fatty liver disease

Indexed keywords

N(G) METHYL DEXTRO ARGININE; NITRIC OXIDE; NITROPRUSSIDE SODIUM; TRIACYLGLYCEROL;

ABDOMINAL FAT; ADULT; ARTICLE; BLOOD VESSEL FUNCTION; BLOOD VESSEL REACTIVITY; BODY TEMPERATURE; CARDIOPULMONARY FUNCTION; CARDIOVASCULAR DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; EXERCISE; FEMALE; HUMAN; LASER DOPPLER FLOWMETRY; LIFESTYLE MODIFICATION; MALE; MICROCIRCULATION; MICRODIALYSIS; NONALCOHOLIC FATTY LIVER; NUCLEAR MAGNETIC RESONANCE IMAGING; OXYGEN CONSUMPTION; PATIENT CARE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RANDOMIZED CONTROLLED TRIAL; SKIN BLOOD FLOW; VASODILATATION; WEIGHT REDUCTION;

CUTANEOUS MICROVESSEL FUNCTION; EXERCISE; EXERCISE TRAINING; MICROVASCULAR FUNCTION; NITRIC OXIDE; NONALCOHOLIC FATTY LIVER DISEASE;

ADULT; CARDIOVASCULAR DISEASES; EXERCISE THERAPY; FATTY LIVER; FEMALE; HOT TEMPERATURE; HUMANS; LASER-DOPPLER FLOWMETRY; MALE; MICROCIRCULATION; MIDDLE AGED; OXYGEN CONSUMPTION; RISK FACTORS; RISK REDUCTION BEHAVIOR; SKIN; TREATMENT OUTCOME;

EID: 84883225713     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00055.2013     Document Type: Article

References (44)

1. Adams LA, Lymp JF, St. Sauver J, Sanderson SO, Lindor KD, Feldstein A, Angulo P. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 129: 113-121, 2005.
2. Black MA, Green DJ, Cable NT. Exercise prevents age-related decline in nitric-oxide-mediated vasodilator function in cutaneous microvessels. J Physiol 586: 3511-3524, 2008.
3. Bonekamp S, Barone B, Clark J, Stewart K. The effects of an exercise training intervention on hepatic steatosis (Abstract). Hepatology 48: 806A, 2008.
4. Bonetti PO, Pumper GM, Higano ST, Holmes DR Jr, Kuvin JT, Lerman A. Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol 44: 2137-2141, 2004.
5. Borg G. Borg's Perceived Exertion and Pain Scales. Champaign, IL: Human Kinetics Publishers, 1998.
6. Brodsky SV, Gealekman O, Chen J, Zhang F, Togashi N, Crabtree M, Gross SS, Nasjletti A, Goligorsky MS. Prevention and reversal of premature endothelial cell senescence and vasculopathy in obesity-induced diabetes by ebselen. Circ Res 94: 377-384, 2004.
7. Bruce RA, Kusumi F, Hosmer D. Maximal oxygen intake and nomographic assessment of functional aerobic impairment in cardiovascular disease. Am Heart J 85: 546-562, 1973.
8. Burkhalter N. [Evaluation of Borg's perceived exertion scale in cardiac rehabilitation]. Rev Lat Am Enfermagem 4: 65-73, 1996.
9. Caballero AE, Arora S, Saouaf R, Lim SC, Smakowski P, Park JY, King GL, LoGerfo FW, Horton ES, Veves A. Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes. Diabetes 48: 1856-1862, 1999.
10. Carberry PA, Shepherd AM, Johnson JM. Resting and maximal forearm skin blood flows are reduced in hypertension. Hypertension 20: 349-355, 1992.
11. Cracowski JL, Minson CT, Salvat-Melis M, Halliwill JR. Methodological issues in the assessment of skin microvascular endothelial function in humans. Trends Pharmacol Sci 27: 503-508, 2006.
12. De Boer MP, Meijer RI, Wijnstok NJ, Jonk AM, Houben AJ, Stehouwer CD, Smulders YM, Eringa EC, Serne EH. Microvascular dysfunction: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension. Microcirculation 19: 5-18, 2012.
13. de Jongh RT, Serné EH, IJzerman RG, de Vries G, Stehouwer CD. Impaired microvascular function in obesity: implications for obesityassociated microangiopathy, hypertension, and insulin resistance. Circulation 109: 2529-2535, 2004.
14. Després JP. Cardiovascular disease under the influence of excess visceral fat. Crit Pathw Cardiol 6: 51-59, 2007.
15. Ekstedt M, Franzen LE, Mathiesen UL, Thorelius L, Holmqvist M, Bodemar G, Kechagias S. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology 44: 865-873, 2006.
16. Green DJ, Carter HH, Fitzsimons MG, Cable NT, Thijssen DH, Naylor LH. Obligatory role of hyperaemia and shear stress in microvascular adaptation to repeated heating in humans. J Physiol 588: 1571-1577, 2010.
17. Green DJ, Jones H, Thijssen D, Cable NT, Atkinson G. Flow-mediated dilation and cardiovascular event prediction: does nitric oxide matter? Hypertension 57: 363-369, 2011.
18. Hambrecht R, Adams V, Erbs S, Linke A, Krankel N, Shu Y, Baither Y, Gielen S, Thiele H, Gummert JF, Mohr FW, Schuler G. Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 107: 3152-3158, 2003.
19. Holowatz LA, Thompson-Torgerson CS, Kenney WL. The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol 105: 370-372, 2008.
20. Holowatz LA, Thompson CS, Minson CT, Kenney WL. Mechanisms of acetylcholine-mediated vasodilatation in young and aged human skin. J Physiol 563: 965-973, 2005.
21. Joannides R, Bellien J, Thuillez C. Clinical methods for the evaluation of endothelial function-a focus on resistance arteries. Fundam Clin Pharmacol 20: 311-320, 2006.
22. Johnson NA, Sachinwalla T, Walton DW, Smith K, Armstrong A, Thompson MW, George J. Aerobic exercise training reduces hepatic and visceral lipids in obese individuals without weight loss. Hepatology 50: 1105-1112, 2009.
23. Jones H, Sprung VS, Pugh CJ, Daousi C, Irwin A, Aziz N, Adams VL, Thomas EL, Bell JD, Kemp GJ, Cuthbertson DJ. Polycystic ovary syndrome with hyperandrogenism is characterized by an increased risk of hepatic steatosis compared with nonhyperandrogenic PCOS phenotypes and healthy controls, independent of obesity and insulin resistance. J Clin Endocrinol Metab 97: 3709-3716, 2012.
24. Joyner MJ, Wilkins BW. Exercise hyperaemia: is anything obligatory but the hyperaemia? J Physiol 583: 855-860, 2007.
25. Kaufman C, Berg K, Noble J, Thomas J. Ratings of perceived exertion of ACSM exercise guidelines in individuals varying in aerobic fitness. Res Q Exerc Sport 77: 122-130, 2006.
26. Kellogg DL Jr, Zhao JL, Coey U, Green JV. Acetylcholine-induced vasodilation is mediated by nitric oxide and prostaglandins in human skin. J Appl Physiol 98: 629-632, 2005.
27. Khan F, Litchfield SJ, Stonebridge PA, Belch JJ. Lipid-lowering and skin vascular responses in patients with hypercholesterolaemia and peripheral arterial obstructive disease. Vasc Med 4: 233-238, 1999.
28. Khan F, Patterson D, Belch JJ, Hirata K, Lang CC. Relationship between peripheral and coronary function using laser Doppler imaging and transthoracic echocardiography. Clin Sci (Lond) 115: 295-300, 2008.
29. Minson CT, Holowatz LA, Wong BJ, Kenney WL, Wilkins BW. Decreased nitric oxide-and axon reflex-mediated cutaneous vasodilation with age during local heating. J Appl Physiol 93: 1644-1649, 2002.
30. Ong JP, Pitts A, Younossi ZM. Increased overall mortality and liverrelated mortality in non-alcoholic fatty liver disease. J Hepatol 49: 608-612, 2008.
31. Perneger TV. What's wrong with Bonferroni adjustments. BMJ 316: 1236-1238, 1998.
32. Petta S, Muratore C, Craxi A. Non-alcoholic fatty liver disease pathogenesis: the present and the future. Dig Liver Dis 41: 615-625, 2009.
33. Rizzoni D, Porteri E, Boari GE, De Ciuceis C, Sleiman I, Muiesan ML, Castellano M, Miclini M, Agabiti-Rosei E. Prognostic significance of small-artery structure in hypertension. Circulation 108: 2230-2235, 2003.
34. Senturk O, Kocaman O, Hulagu S, Sahin T, Aygun C, Konduk T, Celebi A. Endothelial dysfunction in Turkish patients with non-alcoholic fatty liver disease. Intern Med J 38: 183-189, 2008.
35. Shamim-Uzzaman QA, Pfenninger D, Kehrer C, Chakrabarti A, Kacirotti N, Rubenfire M, Brook R, Rajagopalan S. Altered cutaneous microvascular responses to reactive hyperaemia in coronary artery disease: a comparative study with conduit vessel responses. Clin Sci (Lond) 103: 267-273, 2002.
36. Soderberg C, Stal P, Askling J, Glaumann H, Lindberg G, Marmur J, Hultcrantz R. Decreased survival of subjects with elevated liver function tests during a 28-year follow-up. Hepatology 51: 595-602, 2010.
37. Sokolnicki LA, Roberts SK, Wilkins BW, Basu A, Charkoudian N. Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus. Am J Physiol Endocrinol Metab 292: E314-E318, 2007.
38. Sprung VS, Cuthbertson DJ, Pugh CJ, Daousi C, Atkinson G, Aziz NF, Kemp GJ, Green DJ, Cable NT, Jones H. Nitric oxide-mediated cutaneous microvascular function is impaired in polycystic ovary sydrome but can be improved by exercise training. J Physiol 591: 1475-1487, 2013.
39. Szczepaniak LS, Nurenberg P, Leonard D, Browning JD, Reingold JS, Grundy S, Hobbs HH, Dobbins RL. Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288: E462-E468, 2005.
40. van der Heijden GJ, Wang ZJ, Chu ZD, Sauer PJ, Haymond MW, Rodriguez LM, Sunehag AL. A 12-week aerobic exercise program reduces hepatic fat accumulation and insulin resistance in obese, Hispanic adolescents. Obesity (Silver Spring) 18: 384-390, 2010.
41. Vickers AJ, Altman DG. Statistics notes: Analysing controlled trials with baseline and follow up measurements. BMJ 323: 1123-1124, 2001.
42. Villanova N, Moscatiello S, Ramilli S, Bugianesi E, Magalotti D, Vanni E, Zoli M, Marchesini G. Endothelial dysfunction and cardiovascular risk profile in nonalcoholic fatty liver disease. Hepatology 42: 473-480, 2005.
43. Wenner MM, Taylor HS, Stachenfeld NS. Endothelin B receptor contribution to peripheral microvascular function in women with polycystic ovary syndrome. J Physiol 589: 4671-4679, 2011.
44. Wick DE, Roberts SK, Basu A, Sandroni P, Fealey RD, Sletten D, Charkoudian N. Delayed threshold for active cutaneous vasodilation in patients with Type 2 diabetes mellitus. J Appl Physiol 100: 637-641, 2006.