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Journal of Bone and Mineral Metabolism

, Volume 37, Issue 4, pp 694–702 | Cite as

Change of skeletal muscle mass in patients with pheochromocytoma

  • Seung Hun Lee
  • Mi Kyung Kwak
  • Seong Hee Ahn
  • Hyeonmok Kim
  • Yoon Young Cho
  • Sunghwan Suh
  • Kee-Ho Song
  • Jung-Min Koh
  • Jae Hyeon KimEmail author
  • Beom-Jun KimEmail author
Original Article
  • 303 Downloads

Abstract

The effects of catecholamine excess due to pheochromocytoma on body composition, including skeletal muscle mass, are unknown. Here, we investigated the effects of catecholamine metabolites on body composition in subjects with pheochromocytoma. After body compositions using bioelectrical impedance analysis, urinary metanephrine (UM), and urinary normetanephrine (UNM) were measured in 16 patients with pheochromocytoma and 224 patients with nonfunctioning adrenal incidentaloma (NFAI), we compared skeletal muscle mass and fat mass (FM) between the two groups. After adjustments for confounders, UM (β = − 0.171, P = 0.006) and UNM (β = − 0.249, P < 0.001) levels were correlated inversely with skeletal muscle mass index (SMI), but not FM or percentage FM (pFM), in all subjects. Patients with pheochromocytoma had lower ASM by 7.7% (P = 0.022) and SMI by 6.6% (P = 0.001) than patients with NFAI. Conversely, FM and pFM were not statistically different between the two groups. The odds ratio for low skeletal muscle mass in the presence of pheochromocytoma was 10.33 (95% confidence interval, 2.65–40.22). Our results indicate that patients with pheochromocytoma have a reduced skeletal muscle mass and suggest that catecholamine excess has adverse effects on skeletal muscle metabolism.

Keywords

Pheochromocytoma Catecholamine Skeletal muscle Sarcopenia 

Notes

Author contribution

JHK and BJK should be considered senior authors. JHK and BJK had full access to all of the data in the study and take responsibility for the integrity of the data and accuracy of the data analysis. SHL, JHK, and BJK were involved in study conception or design. SHL performed data analysis or interpretation. MKK, SHA, HK, YYC, SS, KHS, and JMK performed data acquisition. SHL, JHK, and BJK were involved in drafting and critical revision of the manuscript for intellectual content. All authors, SHL, MKK, SHA, HK, YYC, SS, KHS, JMK, JHK, and BJK, evaluated the data, reviewed the manuscript, and approved the submission of the manuscript

Funding

This study was supported by a grant from the Asan Institute for Life Sciences (Seoul, Korea, project no. 2018-568), from Dong-A ST (Seoul, Korea, project no. 2011-04-090), and from the Bio & Medical Technology Development Program of the National Research Foundation, funded by the Korean government, MSIP (project no. 2016M3A9E8941329)

Compliance with ethical standards

Conflict of interest

The authors report no potential conflicts of interest.

Research involving human participants

All procedures involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

774_2018_959_MOESM1_ESM.pdf (779 kb)
Supplementary material 1 (PDF 778 kb)

References

  1. 1.
    He W, Goodkind D, Kowal P (2016) An Aging World: 2015. International Population Reports, P95/16-1. US Census Bureau, WashingtonGoogle Scholar
  2. 2.
    Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW et al (2014) Sarcopenia in Asia: consensus report of the asian working group for Sarcopenia. J Am Med Dir Assoc 15:95–101CrossRefPubMedGoogle Scholar
  3. 3.
    Kim YS, Lee Y, Chung YS, Lee DJ, Joo NS, Hong D, Song G, Kim HJ, Choi YJ, Kim KM (2012) Prevalence of sarcopenia and sarcopenic obesity in the korean population based on the fourth korean national health and nutritional examination surveys. J Gerontol A Biol Sci Med Sci 67:1107–1113CrossRefPubMedGoogle Scholar
  4. 4.
    Ryu M, Jo J, Lee Y, Chung YS, Kim KM, Baek WC (2013) Association of physical activity with sarcopenia and sarcopenic obesity in community-dwelling older adults: the fourth Korea national health and nutrition examination survey. Age Ageing 42:734–740CrossRefPubMedGoogle Scholar
  5. 5.
    Chen LK, Lee WJ, Peng LN, Liu LK, Arai H, Akishita M (2016) Recent advances in Sarcopenia research in Asia: 2016 update from the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 17:e761–e767CrossRefGoogle Scholar
  6. 6.
    Okamura T, Nakajima Y, Satoh T, Hashimoto K, Sapkota S, Yamada E, Okada S, Fukuda J, Higuchi T, Tsushima Y, Yamada M (2015) Changes in visceral and subcutaneous fat mass in patients with pheochromocytoma. Metabolism 64:706–712CrossRefPubMedGoogle Scholar
  7. 7.
    Petrak O, Haluzikova D, Kavalkova P, Strauch B, Rosa J, Holaj R, Brabcova Vrankova A, Michalsky D, Haluzik M, Zelinka T, Widimsky J Jr (2013) Changes in energy metabolism in pheochromocytoma. J Clin Endocrinol Metab 98:1651–1658CrossRefPubMedGoogle Scholar
  8. 8.
    Kim YS, Sainz RD, Molenaar P, Summers RJ (1991) Characterization of beta 1- and beta 2-adrenoceptors in rat skeletal muscles. Biochem Pharmacol 42:1783–1789CrossRefPubMedGoogle Scholar
  9. 9.
    Lynch GS, Ryall JG (2008) Role of beta-adrenoceptor signaling in skeletal muscle: implications for muscle wasting and disease. Physiol Rev 88:729–767CrossRefPubMedGoogle Scholar
  10. 10.
    Navegantes LC, Resano NM, Migliorini RH, Kettelhut IC (2000) Role of adrenoceptors and cAMP on the catecholamine-induced inhibition of proteolysis in rat skeletal muscle. Am J Physiol Endocrinol Metab 279:E663–E668CrossRefPubMedGoogle Scholar
  11. 11.
    Kline WO, Panaro FJ, Yang H, Bodine SC (2007) Rapamycin inhibits the growth and muscle-sparing effects of clenbuterol. J Appl Physiol (1985) 102:740–747CrossRefGoogle Scholar
  12. 12.
    Lynch GS, Schertzer JD, Ryall JG (2007) Therapeutic approaches for muscle wasting disorders. Pharmacol Ther 113:461–487CrossRefPubMedGoogle Scholar
  13. 13.
    Beitzel F, Gregorevic P, Ryall JG, Plant DR, Sillence MN, Lynch GS (2004) Beta2-adrenoceptor agonist fenoterol enhances functional repair of regenerating rat skeletal muscle after injury. J Appl Physiol 96:1385–1392CrossRefPubMedGoogle Scholar
  14. 14.
    Hinkle RT, Hodge KM, Cody DB, Sheldon RJ, Kobilka BK, Isfort RJ (2002) Skeletal muscle hypertrophy and anti-atrophy effects of clenbuterol are mediated by the beta2-adrenergic receptor. Muscle Nerve 25:729–734CrossRefPubMedGoogle Scholar
  15. 15.
    Kim YS, Sainz RD, Summers RJ, Molenaar P (1992) Cimaterol reduces beta-adrenergic receptor density in rat skeletal muscles. J Anim Sci 70:115–122CrossRefPubMedGoogle Scholar
  16. 16.
    McElligott MA, Barreto A Jr, Chaung LY (1989) Effect of continuous and intermittent clenbuterol feeding on rat growth rate and muscle. Comp Biochem Physiol C 92:135–138CrossRefPubMedGoogle Scholar
  17. 17.
    Bacurau AV, Jardim MA, Ferreira JC, Bechara LR, Bueno CR Jr, Alba-Loureiro TC, Negrao CE, Casarini DE, Curi R, Ramires PR, Moriscot AS, Brum PC (2009) Sympathetic hyperactivity differentially affects skeletal muscle mass in developing heart failure: role of exercise training. J Appl Physiol 106:1631–1640CrossRefPubMedGoogle Scholar
  18. 18.
    Faber JE (1988) In situ analysis of alpha-adrenoceptors on arteriolar and venular smooth muscle in rat skeletal muscle microcirculation. Circ Res 62:37–50CrossRefPubMedGoogle Scholar
  19. 19.
    Rattigan S, Appleby GJ, Edwards SJ, McKinstry WJ, Colquhoun EQ, Clark MG, Richter EA (1986) Alpha-adrenergic receptors in rat skeletal muscle. Biochem Biophys Res Commun 136:1071–1077CrossRefPubMedGoogle Scholar
  20. 20.
    Lenders JW, Duh QY, Eisenhofer G, Gimenez-Roqueplo AP, Grebe SK, Murad MH, Naruse M, Pacak K, Young WF Jr (2014) Pheochromocytoma and paraganglioma: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 99:1915–1942CrossRefPubMedGoogle Scholar
  21. 21.
    La Batide-Alanore A, Chatellier G, Plouin PF (2003) Diabetes as a marker of pheochromocytoma in hypertensive patients. J Hypertens 21:1703–1707CrossRefPubMedGoogle Scholar
  22. 22.
    Resmini E, Minuto F, Colao A, Ferone D (2009) Secondary diabetes associated with principal endocrinopathies: the impact of new treatment modalities. Acta Diabetol 46:85–95CrossRefPubMedGoogle Scholar
  23. 23.
    Wiesner TD, Bluher M, Windgassen M, Paschke R (2003) Improvement of insulin sensitivity after adrenalectomy in patients with pheochromocytoma. J Clin Endocrinol Metab 88:3632–3636CrossRefPubMedGoogle Scholar
  24. 24.
    Spyroglou A, Adolf C, Hahner S, Quinkler M, Ladurner R, Reincke M, Beuschlein F (2017) Changes in body mass index in pheochromocytoma patients following adrenalectomy. Horm Metab Res 49:208–213CrossRefPubMedGoogle Scholar
  25. 25.
    Lee SH, Song KH, Kim J, Park S, Ahn SH, Kim H, Cho YY, Suh S, Kim BJ, Kim JH, Koh JM (2017) New diagnostic criteria for subclinical hypercortisolism using postsurgical hypocortisolism: the co-work of adrenal research study. Clin Endocrinol 86:10–18 (Oxf) CrossRefGoogle Scholar
  26. 26.
    Cho YY, Song KH, Kim YN, Ahn SH, Kim H, Park S, Suh S, Kim BJ, Lee SY, Chun S, Koh JM, Lee SH, Kim JH (2016) Symptom-dependent cut-offs of urine metanephrines improve diagnostic accuracy for detecting pheochromocytomas in two separate cohorts, compared to symptom-independent cut-offs. Endocrine 54:206–216CrossRefPubMedGoogle Scholar
  27. 27.
    Richards JC, Luckasen GJ, Larson DG, Dinenno FA (2014) Role of alpha-adrenergic vasoconstriction in regulating skeletal muscle blood flow and vascular conductance during forearm exercise in ageing humans. J Physiol 592:4775–4788CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Tuna MM, Imga NN, Dogan BA, Yilmaz FM, Topcuoglu C, Akbaba G, Berker D, Guler S (2014) Non-functioning adrenal incidentalomas are associated with higher hypertension prevalence and higher risk of atherosclerosis. J Endocrinol Invest 37:765–768CrossRefPubMedGoogle Scholar
  29. 29.
    Carson JA, Baltgalvis KA (2010) Interleukin 6 as a key regulator of muscle mass during cachexia. Exerc Sport Sci Rev 38:168–176CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Pedersen BK, Febbraio MA (2012) Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 8:457–465CrossRefGoogle Scholar
  31. 31.
    Frost RA, Nystrom GJ, Lang CH (2004) Epinephrine stimulates IL-6 expression in skeletal muscle and C2C12 myoblasts: role of c-Jun NH2-terminal kinase and histone deacetylase activity. Am J Physiol Endocrinol Metab 286:E809–E817CrossRefPubMedGoogle Scholar
  32. 32.
    Fassnacht M, Arlt W, Bancos I, Dralle H, Newell-Price J, Sahdev A, Tabarin A, Terzolo M, Tsagarakis S, Dekkers OM (2016) Management of adrenal incidentalomas: European society of endocrinology clinical practice guideline in collaboration with the european network for the study of adrenal tumors. Eur J Endocrinol 175:G1–G34CrossRefPubMedGoogle Scholar
  33. 33.
    Hong AR, Kim JH, Park KS, Kim KY, Lee JH, Kong SH, Lee SY, Shin CS, Kim SW, Kim SY (2017) Optimal follow-up strategies for adrenal incidentalomas: reappraisal of the 2016 ESE-ENSAT guidelines in real clinical practice. Eur J Endocrinol 177:475–483CrossRefGoogle Scholar
  34. 34.
    Cases A, Bono M, Gaya J, Jimenez W, Calls J, Esforzado N, Rivera F, Revert L (1995) Reversible decrease of surface beta 2-adrenoceptor number and response in lymphocytes of patients with pheochromocytoma. Clin Exp Hypertens 17:537–549CrossRefPubMedGoogle Scholar
  35. 35.
    Janssen I, Heymsfield SB, Baumgartner RN, Ross R (2000) Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol 89:465–471CrossRefPubMedGoogle Scholar

Copyright information

© The Japanese Society for Bone and Mineral Research and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Seung Hun Lee
    • 1
  • Mi Kyung Kwak
    • 1
  • Seong Hee Ahn
    • 2
  • Hyeonmok Kim
    • 3
  • Yoon Young Cho
    • 4
  • Sunghwan Suh
    • 5
  • Kee-Ho Song
    • 6
  • Jung-Min Koh
    • 1
  • Jae Hyeon Kim
    • 7
    Email author
  • Beom-Jun Kim
    • 1
    Email author
  1. 1.Division of Endocrinology and Metabolism, Department of Medicine, Asan Medical CenterUniversity of Ulsan College of MedicineSeoulSouth Korea
  2. 2.Division of Endocrinology and Metabolism, Department of Medicine, Inha University HospitalInha University School of MedicineIncheonSouth Korea
  3. 3.Department of MedicineSeoul Medical CenterSeoulSouth Korea
  4. 4.Division of Endocrinology and Metabolism, Department of MedicineGyeongsang National University School of MedicineJinjuSouth Korea
  5. 5.Division of Endocrinology and Metabolism, Department of MedicineDong-A University Medical Center, Dong-A, University College of MedicineBusanSouth Korea
  6. 6.Division of Endocrinology and Metabolism, Department of Medicine, Konkuk University Medical CenterKonkuk University School of MedicineSeoulSouth Korea
  7. 7.Division of Endocrinology and Metabolism, Department of Medicine, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulSouth Korea

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