Pilot study on the effects of a 2-week hiking vacation at moderate versus low altitude on plasma parameters of carbohydrate and lipid metabolism in patients with metabolic syndrome

Ivana Gutwenger, Georg Hofer, Anna K Gutwenger, Marco Sandri, Christian J Wiedermann, Ivana Gutwenger, Georg Hofer, Anna K Gutwenger, Marco Sandri, Christian J Wiedermann

Abstract

Background: Hypoxic and hypobaric conditions may augment the beneficial influence of training on cardiovascular risk factors. This pilot study aimed to explore for effects of a two-week hiking vacation at moderate versus low altitude on adipokines and parameters of carbohydrate and lipid metabolism in patients with metabolic syndrome.

Methods: Fourteen subjects (mean age: 55.8 years, range: 39 - 69) with metabolic syndrome participated in a 2-week structured training program (3 hours of guided daily hiking 4 times a week, training intensity at 55-65% of individual maximal heart rate; total training time, 24 hours). Participants were divided for residence and training into two groups, one at moderate altitude (1,900 m; n = 8), and the other at low altitude (300 m; n = 6). Anthropometric, cardiovascular and metabolic parameters were measured before and after the training period.

Results: In study participants, training overall reduced circulating levels of total cholesterol (p = 0.024), low-density lipoprotein cholesterol (p = 0.025) and adiponectin (p < 0.001). In the group training at moderate altitude (n = 8), lowering effects on circulating levels were significant not only for total cholesterol, low-density-lipoprotein cholesterol and adiponectin (all, p < 0.05) but also for triglycerides (p = 0.025) and leptin (p = 0.015), whereas in the low altitude group (n = 6), none of the lipid parameters was significantly changed (each p > 0.05). Hiking-induced relative changes of triglyceride levels were positively associated with reductions in leptin levels (p = 0.006). As compared to 300 m altitude, training at 1,900 m showed borderline significant differences in the pre-post mean reduction rates of triglyceride (p = 0.050) and leptin levels (p = 0.093).

Conclusions: Preliminary data on patients with metabolic syndrome suggest that a 2-week hiking vacation at moderate altitude may be more beneficial for adipokines and parameters of lipid metabolism than training at low altitude. In order to draw firm conclusions regarding better corrections of dyslipidemia and metabolic syndrome by physical exercise under mild hypobaric and hypoxic conditions, a sufficiently powered randomized clinical trial appears warranted.

Trial registration: ClinicalTrials.gov ID NCT02013947 (first received November 6, 2013).

Figures

Figure 1
Figure 1
Pre- and post-training change (percentage) in leptin and triglyceride levels.

References

    1. Alberti KGMM, Zimmet P, Shaw J. Metabolic syndrome – a new world-wide definition. A consensus statement from the international diabetes federation. Diabet Med. 2006;23:469–80. doi: 10.1111/j.1464-5491.2006.01858.x.
    1. National Cholesterol Education Program Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on the Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation. 2002;106:3143–421.
    1. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; american heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation. 2009;120:1640–5. doi: 10.1161/CIRCULATIONAHA.109.192644.
    1. Pérez-López FR, Chedraui P, Gilbert JJ, Pérez-Roncero G. Cardiovascular risk in menopausal women and prevalent related co-morbid conditions: facing the post-Women’s health initiative era. Fertil Steril. 2009;92:1171–86. doi: 10.1016/j.fertnstert.2009.06.032.
    1. Esposito K, Chiodini P, Colao A, Lenzi A, Giugliano D. Metabolic syndrome and risk of cancer: a systematic review and meta-analysis. Diabetes Care. 2012;35:2402–11. doi: 10.2337/dc12-0336.
    1. Lin JW, Caffrey JL, Chang MH, Lin YS. Sex, menopause, metabolic syndrome, and all-cause and cause-specific mortality–cohort analysis from the third national health and nutrition examination survey. J Clin Endocrinol Metab. 2010;95:4258–67. doi: 10.1210/jc.2010-0332.
    1. Chedraui P, Pérez-López FR, Blümel JE, Hidalgo L, Barriga J. Hyperglycemia in postmenopausal women screened for the metabolic syndrome is associated to increased sexual complaints. Gynecol Endocrinol. 2010;26:86–92. doi: 10.3109/09513590903184092.
    1. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 1999;257:79–83. doi: 10.1006/bbrc.1999.0255.
    1. Qiao L, Zou C, van der Westhuyzen DR, Shao J. Adiponectin reduces plasma triglyceride by increasing VLDL triglyceride catabolism. Diabetes. 2008;57:1824–33. doi: 10.2337/db07-0435.
    1. Matsuura F, Oku H, Koseki M, Sandoval JC, Yuasa-Kawase M, Tsubakio-Yamamoto K, et al. Adiponectin accelerates reverse cholesterol transport by increasing high density lipoprotein assembly in the liver. Biochem Biophys Res Commun. 2007;358:1091–5. doi: 10.1016/j.bbrc.2007.05.040.
    1. Oku H, Matsuura F, Koseki M, Sandoval JC, Yuasa-Kawase M, Tsubakio-Yamamoto K, et al. Adiponectin deficiency suppresses ABCA1 expression and ApoA-I synthesis in the liver. FEBS Lett. 2007;581:5029–33. doi: 10.1016/j.febslet.2007.09.038.
    1. Iwashima Y, Katsuya T, Ishikawa K, Ouchi N, Ohishi M, Sugimoto K, et al. Hypoadiponectinemia is an independent risk factor for hypertension. Hypertension. 2004;43:1318–23. doi: 10.1161/01.HYP.0000129281.03801.4b.
    1. Ryo M, Nakamura T, Kihara S, Kumada M, Shibazaki S, Takahashi M, et al. Adiponectin as a biomarker of the metabolic syndrome. Circ J. 2004;68:975–81. doi: 10.1253/circj.68.975.
    1. Mattu HS, Randeva HS. Role of adipokines in cardiovascular disease. J Endocrinol. 2013;216:T17–36. doi: 10.1530/JOE-12-0232.
    1. Schindler TH, Cardenas J, Prior JO, Facta AD, Kreissl MC, Zhang XL, et al. Relationship between increasing body weight, insulin resistance, inflammation, adipocytokine leptin, and coronary circulatory function. J Am Coll Cardiol. 2006;47:1188–95. doi: 10.1016/j.jacc.2005.10.062.
    1. Gruzdeva O, Uchasova E, Belik E, Dyleva Y, Shurygina E, Barbarash O. Lipid, adipokine and ghrelin levels in myocardial infarction patients with insulin resistance. BMC Cardiovasc Disord. 2014;14:7. doi: 10.1186/1471-2261-14-7.
    1. Vissers D, Hens W, Taeymans J, Baeyens JP, Poortmans J, Van Gaal L. The effect of exercise on visceral adipose tissue in overweight adults: a systematic review and meta-analysis. PLoS One. 2013;8:e56415. doi: 10.1371/journal.pone.0056415.
    1. Pattyn N, Cornelissen VA, Eshghi SR, Vanhees L. The effect of exercise on the cardiovascular risk factors constituting the metabolic syndrome: a meta-analysis of controlled trials. Sports Med. 2013;43:121–33. doi: 10.1007/s40279-012-0003-z.
    1. Pescatello LS, Blanchard BE, Van Heest JL, Maresh CM, Gordish-Dressman H, Thompson PD. The metabolic syndrome and the immediate antihypertensive effects of aerobic exercise: a randomized control design. BMC Cardiovasc Disord. 2008;8:12. doi: 10.1186/1471-2261-8-12.
    1. Golbidi S, Laher I. Exercise induced adipokine changes and the metabolic syndrome. J Diabetes Res. 2014;2014:726861. doi: 10.1155/2014/726861.
    1. Wu TY, Ding SQ, Liu JL, Yu MT, Jia JH, Chai ZC, et al. Who should not go high: chronic disease and work at altitude during construction of the Qinghai-Tibet railroad. High Alt Med Biol. 2007;8:88–107. doi: 10.1089/ham.2007.1015.
    1. Ri-Li G, Chase PJ, Witkowski S, Wyrick BL, Stone JA, Levine BD, et al. Obesity: associations with acute mountain sickness. Ann Intern Med. 2003;139:253–7. doi: 10.7326/0003-4819-139-4-200308190-00007.
    1. Boyer SJ, Blume FD. Weight-loss and changes in body composition at high altitude. J Appl Physiol. 1984;57:1580–5.
    1. Netzer NC, Chytra R, Küpper T. Low intense physical exercise in normobaric hypoxia leads to more weight loss in obese people than low intense physical exercise in normobaric sham hypoxia. Sleep Breath. 2008;12:129–34. doi: 10.1007/s11325-007-0149-3.
    1. Workman C, Basset FA. Post-metabolic response to passive normobaric hypoxic exposure in sedentary overweight males: a pilot study. Nutr Metab (Lond) 2012;9:103. doi: 10.1186/1743-7075-9-103.
    1. Cai Z, Luo W, Zhan H, Semenza GL. Hypoxia-inducible factor 1 is required for remote ischemic preconditioning of the heart. Proc Natl Acad Sci U S A. 2013;110:17462–7. doi: 10.1073/pnas.1317158110.
    1. Howangyin KY, Silvestre JS. Diabetes mellitus and ischemic diseases: molecular mechanisms of vascular repair dysfunction. Arterioscler Thromb Vasc Biol. 2014;34:1126–35. doi: 10.1161/ATVBAHA.114.303090.
    1. Burtscher M. Effects of living at higher altitudes on mortality: a narrative review. Aging Dis. 2013;5:274–80.
    1. Stöwhas AC, Latshang TD, Lo Cascio CM, Lautwein S, Stadelmann K, Tesler N, et al. Effects of acute exposure to moderate altitude on vascular function, metabolism and systemic inflammation. PLoS One. 2013;8:e70081. doi: 10.1371/journal.pone.0070081.
    1. Haufe S, Wiesner S, Engeli S, Luft FC, Jordan J. Influences of normobaric hypoxia training on metabolic risk markers in human subjects. Med Sci Sports Exerc. 2008;40:1939–44. doi: 10.1249/MSS.0b013e31817f1988.
    1. Schobersberger W, Schmid P, Lechleitner M, von Duvillard SP, Hörtnagl H, Gunga HC, et al. The effects of moderate altitude (1,700 m) on cardiovascular and metabolic variables in patients with metabolic syndrome. Eur J Appl Physiol. 2000;2003(88):506–14.
    1. Greie S, Humpeler E, Gunga HC, Koralewski E, Klingler A, Mittermayr M, et al. Improvement of metabolic syndrome markers through altitude specific hiking vacations. J Endocrinol Invest. 2006;29:497–504. doi: 10.1007/BF03344138.
    1. Mair J, Hammerer-Lercher A, Mittermayr M, Klingler A, Humpeler E, Pachinger O, et al. 3-week hiking holidays at moderate altitude do not impair cardiac function in individuals with metabolic syndrome. Int J Cardiol. 2008;123:186–8. doi: 10.1016/j.ijcard.2006.11.127.
    1. Neumayr G, Fries D, Mittermayer M, Humpeler E, Klingler A, Schobersberger W, Spiesberger R, Pokan R, Schmid P: Effects of hiking at moderate and low altitude on cardiovascular parameters in male patients with metabolic syndrome: Austrian Moderate Altitude Study. Wilderness Environ Med. 2014, S1080-6032(14)00006-4.
    1. Sakurai T, Ogasawara J, Kizaki T, Sato S, Ishibashi Y, Takahashi M, et al. The effects of exercise training on obesity-induced dysregulated expression of adipokines in white adipose tissue. Int J Endocrinol. 2013;2013:801743. doi: 10.1155/2013/801743.
    1. Bonate PL. Analysis of pretest-posttest designs. Boca Raton: Chapman & Hall/CRC; 2000.
    1. Lavie CJ, Swift DL. Clinical strategies for managing dyslipidemias: emphasis on physical activity and exercise training. Am J Lifestyle Med. 2014;8:235–8. doi: 10.1177/1559827614528654.
    1. Durstine JL, Grandjean PW, Davis PG, Ferguson MA, Alderson NL, DuBose KD. Blood lipid and lipoprotein adaptations to exercise: a quantitative analysis. Sports Med. 2001;31:1033–62. doi: 10.2165/00007256-200131150-00002.
    1. Farrell PA, Barboriak J. The time course of alterations in plasma lipid and lipoprotein concentrations during eight weeks of endurance training. Atherosclerosis. 1980;37:231–8. doi: 10.1016/0021-9150(80)90008-8.
    1. Tomiyasu K, Ishikawa T, Ikewaki K. Effects of exercise on plasma lipases and cholesterol ester transfer protein activities in normolipidemic male subjects. Nutr Metab Cardiovasc Dis. 1996;6:13–20.
    1. Després JP, Moorjani S, Tremblay A, Poehlman ET, Lupien PJ, Nadeau A, et al. Heredity and changes in plasma lipids and lipoproteins after short-term exercise training in men. Arteriosclerosis. 1988;8:402–9. doi: 10.1161/01.ATV.8.4.402.
    1. Thompson PD, Crouse SF, Goodpaster B, Kelley D, Moyna N, Pescatello L. The acute versus the chronic response to exercise. Med Sci Sports Exerc. 2001;33(6 Suppl):S438–S445. doi: 10.1097/00005768-200106001-00012.
    1. Dressendorfer RH, Wade CE, Hornick C, Timmis GC. High-density lipoprotein-cholesterol in marathon runners during a 20-day road race. JAMA. 1982;247:1715–7. doi: 10.1001/jama.1982.03320370029024.
    1. Crouse SF, O'Brien BC, Grandjean PW, Lowe RC, Rohack JJ, Green JS. Effects of training and a single session of exercise on lipids and apolipoproteins in hypercholesterolemic men. J Appl Physiol (1985) 1997;83:2019–2028.
    1. Cullinane E, Siconolfi S, Saritelli A, Thompson PD. Acute decrease in serum triglycerides with exercise: is there a threshold for an exercise effect? Metabolism. 1982;31:844–7. doi: 10.1016/0026-0495(82)90085-3.
    1. Ferguson MA, Alderson NL, Trost SG, Essig DA, Burke JR, Durstine JL. Effects of four different single exercise sessions on lipids, lipoproteins, and lipoprotein lipase. J Appl Physiol (1985) 1998;85:1169–1174.
    1. Gill JM, Herd SL, Tsetsonis NV, Hardman AE. Are the reductions in triacylglycerol and insulin levels after exercise related? Clin Sci (Lond) 2002;102:223–31. doi: 10.1042/CS20010204.
    1. Burton FL, Malkova D, Caslake MJ, Gill JM. Energy replacement attenuates the effects of prior moderate exercise on postprandial metabolism in overweight/obese men. Int J Obes (Lond) 2008;32:481–9. doi: 10.1038/sj.ijo.0803754.
    1. Harrison M, O'Gorman DJ, McCaffrey N, Hamilton MT, Zderic TW, Carson BP, Moyna NM. Influence of acute exercise with and without carbohydrate replacement on postprandial lipid metabolism. J Appl Physiol (1985) 2009;106:943–949. doi: 10.1152/japplphysiol.91367.2008.
    1. Saunders TJ, Palombella A, McGuire KA, Janiszewski PM, Després JP, Ross R. Acute exercise increases adiponectin levels in abdominally obese men. J Nutr Metab. 2012;2012:148729.
    1. Ackel-D’Elia C, Carnier J, Bueno CR, Jr, Campos RM, Sanches PL, Clemente AP, et al. Effects of different physical exercises on leptin concentration in obese adolescents. Int J Sports Med. 2014;35:164–71.
    1. Kanaley JA, Fenicchia LM, Miller CS, Ploutz-Synder LL, Weinstock RS, Carhart R, et al. Resting leptin responses to acute and chronic resistance training in type 2 diabetic men and women. Int J Obes Relat Metab Disord. 2001;25:1474–80. doi: 10.1038/sj.ijo.0801797.
    1. Phillips MD, Patrizi RM, Cheek DJ, Wooten JS, Barbee JJ, Mitchell JB. Resistance training reduces subclinical inflammation in obese, postmenopausal women. Med Sci Sports Exerc. 2012;44:2099–110. doi: 10.1249/MSS.0b013e3182644984.
    1. Hickey MS, Houmard JA, Considine RV, Tyndall GL, Midgette JB, Gavigan KE, et al. Gender-dependent effects of exercise training on serum leptin levels in humans. Am J Physiol. 1997;272:E562–6.
    1. Wee J, Climstein M: Hypoxic training: Clinical benefits on cardiometabolic risk factors. J Sci Med Sport. 2013. S1440-2440(13)00478-7.
    1. Chen SM, Lin HY, Kuo CH. Altitude training improves glycemic control. Chin J Physiol. 2013;54:193–8.
    1. Lee WC, Chen JJ, Ho HY, Hou CW, Liang MP, Shen YW, et al. Short-term altitude mountain living improves glycemic control. High Alt Med Biol. 2003;4:81–91. doi: 10.1089/152702903321489013.
    1. Do R, Willer CJ, Schmidt EM, Sengupta S, Gao C, Peloso GM, et al. Common variants associated with plasma triglycerides and risk for coronary artery disease. Nat Genet. 2013;45:1345–52. doi: 10.1038/ng.2795.
    1. Tall AR. Exercise to reduce cardiovascular risk: how much is enough? N Engl J Med. 2002;347:1522–4. doi: 10.1056/NEJMe020117.
    1. Chan DC, Barrett PH, Watts GF. The metabolic and pharmacologic bases for treating atherogenic dyslipidaemia. Best Pract Res Clin Endocrinol Metab. 2014;28:369–85. doi: 10.1016/j.beem.2013.10.001.
    1. Fatouros IG, Tournis S, Leontsini D, Jamurtas AZ, Sxina M, Thomakos P, et al. Leptin and adiponectin responses in overweight inactive elderly following resistance training and detraining are intensity related. J Clin Endocrinol Metab. 2005;90:5970–7. doi: 10.1210/jc.2005-0261.
    1. Fatouros IG, Chatzinikolaou A, Tournis S, Nikolaidis MG, Jamurtas AZ, Douroudos II, et al. Intensity of resistance exercise determines adipokine and resting energy expenditure responses in overweight elderly individuals. Diabetes Care. 2009;32:2161–7. doi: 10.2337/dc08-1994.
    1. Kraemer RR, Chu H, Castracane VD. Leptin and exercise. Exp Biol Med (Maywood) 2002;227:701–8.
    1. Barwell ND, Malkova D, Moran CN, Cleland SJ, Packard CJ, Zammit VA, et al. Exercise training has greater effects on insulin sensitivity in daughters of patients with type 2 diabetes than in women with no family history of diabetes. Diabetologia. 2008;51:1912–9. doi: 10.1007/s00125-008-1097-6.
    1. Sattar N, Wannamethee G, Sarwar N, Chernova J, Lawlor DA, Kelly A, et al. Leptin and coronary heart disease: prospective study and systematic review. J Am Coll Cardiol. 2009;53:167–75. doi: 10.1016/j.jacc.2008.09.035.
    1. Cabrera de León A, González DA, Méndez LI, Aguirre-Jaime A, del Cristo Rodríguez Pérez M, Coello SD, Trujillo IC. Leptin and altitude in the cardiovascular diseases. Obes Res. 2004;12:1492–1498. doi: 10.1038/oby.2004.186.
    1. Roels B, Thomas C, Bentley DJ, Mercier J, Hayot M, Millet G. Effects of intermittent hypoxic training on amino and fatty acid oxidative combustion in human permeabilized muscle fibers. J Appl Physiol (1985) 2007;102:79–86. doi: 10.1152/japplphysiol.01319.2005.
    1. Kon M, Ikeda T, Homma T, Akimoto T, Suzuki Y, Kawahara T. Effects of acute hypoxia on metabolic and hormonal responses to resistance exercise. Med Sci Sports Exerc. 2010;42:1279–85. doi: 10.1249/MSS.0b013e3181ce61a5.
    1. Wiesner S, Haufe S, Engeli S, Mutschler H, Haas U, Luft FC, et al. Influences of normobaric hypoxia training on physical fitness and metabolic risk markers in overweight to obese subjects. Obesity (Silver Spring) 2010;18:116–20. doi: 10.1038/oby.2009.193.
    1. Haffner SM, Miettinen H, Mykkänen L, Karhapää P, Rainwater DL, Laakso M. Leptin concentrations and insulin sensitivity in normoglycemic men. Int J Obes Relat Metab Disord. 1997;21:393–9. doi: 10.1038/sj.ijo.0800419.
    1. Fischer S, Hanefeld M, Haffner SM, Fusch C, Schwanebeck U, Köhler C, et al. Insulin-resistant patients with type 2 diabetes mellitus have higher serum leptin levels independently of body fat mass. Acta Diabetol. 2002;39:105–10. doi: 10.1007/s005920200027.
    1. Crunkhorn S. Metabolic disease: exercise hormone fights metabolic disease. Nat Rev Drug Discov. 2012;11:189. doi: 10.1038/nrd3686.
    1. Rosen ED, Spiegelman BM. What we talk about when we talk about fat. Cell. 2014;156:20–44. doi: 10.1016/j.cell.2013.12.012.
    1. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481:463–8. doi: 10.1038/nature10777.
    1. Whittle AJ, Carobbio S, Martins L, Slawik M, Hondares E, Vázquez MJ, et al. BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. Cell. 2012;149:871–85. doi: 10.1016/j.cell.2012.02.066.
    1. Crujeiras AB, Pardo M, Arturo RR, Navas-Carretero S, Zulet MA, Martínez JA, et al. Longitudinal variation of circulating irisin after an energy restriction-induced weight loss and following weight regain in obese men and women. Am J Hum Biol. 2014;26:198–207. doi: 10.1002/ajhb.22493.
    1. Crujeiras AB, Pardo M, Casanueva FF. Irisin: ‘fat’ or artefact. Clin Endocrinol (Oxf). 2014. doi: 10.1111/cen.12627. [Epub ahead of print]
    1. Strauss-Blasche G, Riedmann B, Schobersberger W, Ekmekcioglu C, Riedmann G, Waanders R, et al. Vacation at moderate and low altitude improves perceived health in individuals with metabolic syndrome. J Travel Med. 2004;11:300–4. doi: 10.2310/7060.2004.19106.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe