Skip to main content
SpringerLink
Log in

Adult individuals with congenital, untreated, severe isolated growth hormone deficiency have satisfactory muscular function

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

While growth hormone (GH) and the insulin-like growth factor type I (IGF-I) are known to exert synergistic actions on muscle anabolism, the consequences of prolonged GH deficiency (GHD) on muscle function have not been well defined. We have previously described a large cohort of subjects with isolated GHD (IGHD) caused by a mutation in the GH-releasing hormone receptor gene, with low serum levels of GH and IGF-I. The aim of this study was to assess muscular function in these IGHD subjects.

Methods

A total of 31 GH-naïve IGHD (16 males) and 40 control (20 males) subjects, matched by age and degree of daily physical activity, were enrolled. Fat free mass was measured by bioelectrical impedance; muscle strength by dynamometry of handgrip, trunk extension, and knee extension; myoelectric activity and muscle fatigue by fractal dimension; conduction velocity in vastus medialis, rectus femoris, and vastus lateralis muscles by surface electromyography.

Results

The IGHD group showed higher knee extension strength both when corrected for weight and fat free mass, and higher handgrip and trunk extension strength corrected by fat free mass. They also exhibit higher conduction velocity of the muscles vastus medialis, rectus femoris, and vastus lateralis, but lower free fat mass and myoelectric activity of the vastus medialis, rectus femoris and vastus lateralis. There were no differences between the two groups in fractal dimension in all studied muscles.

Conclusion

Individuals with untreated IGHD have better muscle strength parameters adjusted for weight and fat free mass than controls. They also exhibit greater peripheral resistance to fatigue, demonstrating satisfactory muscle function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. J. Trezise, N. Collier, A.J. Blazevich, Anatomical and neuromuscular variables strongly predict maximum knee extension torque in healthy men. Eur. J. Appl. Physiol. 116, 1159–1177 (2016)

    Article  CAS  PubMed  Google Scholar 

  2. T.S. Gross, S.L. Poliachik, J. Prasad, S.D. Bain, The effect of muscle dysfunction on bone mass and morphology. J. Musculoskelet. Neuron. Interact. 10, 25–34 (2010)

    CAS  Google Scholar 

  3. J.B. Tyrovola, The ‘Mechanostat’ principle and the osteoprotegerin-OPG/RANKL/RANK system PART II. The role of the hypothalamic - pituitary axis. J. Cell. Biochem. 966, 1–20 (2016)

    Google Scholar 

  4. Y.H. Song, J.L. Song, P. Delafontaine, M.P. Godard, The therapeutic potential of IGF-I in skeletal muscle repair. Trends Endocrinol. Metab. 24, 310–319 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. C.Q. Gao, R. Zhi, Z. Yang, H.C. Li, H.C. Yan, X.Q. Wang, Low dose of IGF-I increases cell size of skeletal muscle satellite cells via Akt/S6K signaling pathway. J. Cell. Biochem. 116, 2637–2648 (2015)

    Article  CAS  PubMed  Google Scholar 

  6. J.C. Chow, P.R. Ling, Z. Qu, L. Laviola, A. Ciccarone, B.R. Bistrian, R.J. Smith, Growth hormone stimulates tyrosine phosphorylation of JAK2 and STAT5, but not insulin receptor substrate-1 or SHC proteins in liver and skeletal muscle of normal rats in vivo. Endocrinology 137, 2880–2886 (1996)

    Article  CAS  PubMed  Google Scholar 

  7. X. Ge, J. Yu, H. Jiang, Growth hormone stimulates protein synthesis in bovine skeletal muscle cells without altering insulin-like growth factor-I mRNA expression. J. Anim. Sci. 90, 1126–1133 (2012)

    Article  CAS  PubMed  Google Scholar 

  8. V. Chikani, K.K.Y. Ho, Action of GH on skeletal muscle function: molecular and metabolic mechanisms. J. Mol. Endocrinol. 52, 107–123 (2013)

    Article  CAS  Google Scholar 

  9. Y. Wang, D.D. Bikle, W. Chang, Autocrine and paracrine actions of IGF-I signaling in skeletal development. Bone Res. 1, 249–259 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. D.D. Bikle, C. Tahimic, W. Chang, Y. Wang, A. Philippou, E.R. Barton, Role of IGF-I signaling in muscle bone interactions. Bone 80, 79–88 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. D.S. Kim, E. Itoh, K. Iida, M.O. Thorner, Growth hormone icreases mRNA Levels of PPAR δ and Foxo1 in skeletal muscle of growth hormone deficient lit / lit mice. Endocr. J. 56, 141–147 (2009)

    Article  CAS  PubMed  Google Scholar 

  12. E.O. List, L. Sackmann-Sala, D.E. Berryman, K. Funk, B. Kelder, E.S. Gosney, S. Okada, J. Ding, D. Cruz-Topete, J.J. Kopchick, Endocrine parameters and phenotypes of the growth hormone receptor gene disrupted (GHR−/−) mouse. Endocr. Rev. 32, 356–386 (2011)

    Article  CAS  PubMed  Google Scholar 

  13. K.T. Coschigano, A.N. Holland, M.E. Riders, E.O. List, A. Flyvbjerg, J.J. Kopchick, Deletion, but not antagonism, of the mouse growth hormone receptor results in severely decreased body weights, insulin, and insulin-like growth factor I levels and increased life span. Endocrinology 144, 3799–3810 (2003)

    Article  CAS  PubMed  Google Scholar 

  14. R. Basu, Y. Qian, J.J. Kopchick, Mechanisms in endocrinology: lessons from growth hormone receptor gene disrupted mice: are there benefits of endocrine defects? Eur. J. Endocrinol. 181, 155–181 (2018)

    Article  Google Scholar 

  15. S. Shibata, C. Ueno, T. Ito, K. Yamanouchi, T. Matsuwaki, M. Nishihara, Skeletal muscle growth defect in human growth hormone transgenic rat is accompanied by phenotypic changes in progenitor cells. Age 32, 239–253 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. N. Improda, D. Capalbo, A. Esposito, M. Salerno, Muscle and skeletal health in children and adolescents with GH deficiency. Best. Pract. Res. Clin. Endocrinol. Metab. 30, 771–783 (2016)

    Article  CAS  PubMed  Google Scholar 

  17. L.J. Woodhouse, A. Mukherjee, S.M. Shalet, S. Ezzat, The influence of growth hormone status on physical impairments, functional limitations, and health-related quality of life in adults. Endocr. Rev. 27, 287–317 (2006)

    Article  CAS  PubMed  Google Scholar 

  18. A. Sartorio, F. Agosti, A.D. Col, G. Mazzilli, N. Marazzi, C. Busti, R. Galli, C.L. Lafortuna, Muscle strength and power, maximum oxygen consumption, and body composition in middle-aged short-stature adults with childhood-onset growth harmone deficiency. Arch. Med. Res. 39, 78–83 (2008)

    Article  PubMed  Google Scholar 

  19. W.M. Widdowson, J. Gibney, The effect of growth hormone (GH) replacement on muscle strength in patients with GH-deficiency: A meta-analysis. Clin. Endocrinol. (Oxf.). 72, 787–792 (2010)

    Article  CAS  PubMed  Google Scholar 

  20. M.J. Modesto, N.M. Amer, O. Erichsen, S. Hernandez, C.D. Santos, J.A.R. Carvalho, R.M. Pereira, S.N. França, L. Lacerda, Muscle strength and body composition during the transition phase in patients treated with recombinant GH to final height. J. Pediatr. Endocrinol. Metab. 27, 813–820 (2014)

    Google Scholar 

  21. K. Hermansen, M. Bengtsen, M. Kjær, P. Vestergaard, J.O.L. Jørgensen, Impact of GH administration on athletic performance in healthy young adults: a systematic review and meta-analysis of placebo-controlled trials. Growth Horm. IGF Res. 34, 38–44 (2017)

    Article  CAS  PubMed  Google Scholar 

  22. R. Salvatori, C.Y. Hayashida, M.H. Aguiar-Oliveira, J.A. Phillips, A.H.O. Souza, R.G. Gondo, S.P.A. Toledo, M.M. Conceicão, M. Prince, H.G. Maheshwari, G. Baumann, M.A. Levine, Familial dwarfism due to a novel mutation of the growth hormone-releasing hormone receptor gene. J. Clin. Endocrinol. Metab. 84, 917–923 (1999)

    CAS  PubMed  Google Scholar 

  23. M.H. Aguiar-Oliveira, M.S. Gill, F. Miraki-Moud, C.A. Menezes, A.H.O. Souza, C.E. Martinelli, F.A. Pereira, R. Salvatori, M.A. Levine, S.M. Shalet, C. Camacho-Hubner, P.E. Clayton, Effect of severe growth hormone (GH) deficiency due to a mutation in the GH-releasing hormone receptor on Insulin-Like Growth Factors (IGFs), IGF-Binding Proteins, and Ternary Complex Formation Throughout Life. J. Clin. Endocrinol. Metab. 84, 4118–4126 (1999)

    CAS  PubMed  Google Scholar 

  24. M.H. Aguiar-Oliveira, A.H.O. Souza, C.R.P. Oliveira, V.C. Campos, L.A. Oliveira-Neto, R. Salvatori, The multiple facets of GHRH/GH/IGF-I axis: lessons from lifetime, untreated, isolated GH deficiency due to a GHRH receptor gene mutation. Eur. J. Endocrinol. 177, 85–97 (2017)

    Article  Google Scholar 

  25. M.B. Gois-Junior, R. Salvatori, M.H. Aguiar-Oliveira, F.A. Pereira, C.R.P. Oliveira, L.A. Oliveira-Neto, R.M.C. Pereira, A.H.O. Souza, E.V. Melo, F.J.A. Paula, The consequences of growth hormone-releasing hormone receptor haploinsufficiency for bone quality and insulin resistance. Clin. Endocrinol. (Oxf.). 77, 379–384 (2012)

    Article  CAS  Google Scholar 

  26. C.C. Epitácio-Pereira, G.M.F. Silva, R. Salvatori, J.A.M. Santana, F.A. Pereira, M.B. Gois-Junior, A.V.O. Britto, C.R.P. Oliveira, A.H.O. Souza, E.G. Santos, V.C. Campos, R.M.C. Pereira, E.H.O. Valença, R.A.A. Barbosa, M.I.T. Farias, F.J.A. Paula, T.V. Ribeiro, M.C.P. Oliveira, M.H. Aguiar-Oliveira, Isolated GH deficiency due to a GHRH receptor mutation causes hip joint problems and genu valgum, and reduces size but not density of trabecular and mixed bone. J. Clin. Endocrinol. Metab. 98, 1710–1715 (2013)

    Article  CAS  Google Scholar 

  27. J.A.R. Barbosa, R. Salvatori, C.R.P. Oliveira, R.M.C. Pereira, C.T. Farias, A.V.O. Britto, N.T. Farias, A. Blackford, M.H. Aguiar-Oliveira, Quality of life in congenital, untreated, lifetime isolated growth hormone deficiency. Psychoneuroendocrinology 34, 894–900 (2009)

    Article  CAS  PubMed  Google Scholar 

  28. M.H. Aguiar-Oliveira, F.T. Oliveira, R.M.C. Pereira, C.R.P. Oliveira, A. Blackford, E.H.O. Valenca, E.G. Santos, M.B. Gois-Junior, R.A. Meneguz-Moreno, V.P. Araujo, L.A. Oliveira-Neto, R.P. Almeida, M.A. Santos, N.T. Farias, D.C.R. Silveira, G.W. Cabral, F.R. Calazans, J.D. Seabra, T.F. Lopes, E.O. Rodrigues, L.A. Porto, I.P. Oliveira, E.V. Melo, M. Martari, R. Salvatori, Longevity in untreated congenital growth hormone deficiency due to a homozygous mutation in the GHRH receptor gene. J. Clin. Endocrinol. Metab. 95, 714–721 (2010)

    Article  CAS  PubMed  Google Scholar 

  29. World Health Organization - Measuring obesity: classification, and description of anthropometric data. Copenhagen: World Health Organization. 1988.

  30. IPAQ Research Committee. Guidelines for data processing and analysis of the international physical activity questionnaire (IPAQ) short and long forms. In: International physical activity questionnaire (2005)

  31. J.R. Moon, J.R. Stout, A.E. Smith-Ryan, K.L. Kendall, D.H. Fukuda, J.T. Cramer, S.E. Moon, Tracking fat-free mass changes in elderly men and women using single-frequency bioimpedance and dual-energy X-ray absorptiometry: a four-compartment model comparison. Eur. J. Clin. Nutr. 67, 40–46 (2013)

    Article  Google Scholar 

  32. U.G. Kyle, I. Bosaeus, A.D. Lorenzo, P. Deurenberg, M. Elia, J.M. Gómez, B.L. Heitmann, L. Kent-Smith, J.C. Melchior, M. Pirlich, H. Scharfetter, A.M.W.J. Schols, C. Pichard, Bioelectrical impedance analysis - Part I: review of principles and methods. Clin. Nutr. 23, 1226–1243 (2004)

    Article  PubMed  Google Scholar 

  33. G. Sergi, M. Rui, B. Stubbs, N. Veronese, E. Manzato, Measurement of lean body mass using bioelectrical impedance analysis: a consideration of the pros and cons. Aging Clin. Exp. Res. 29, 591–597 (2017)

    Article  PubMed  Google Scholar 

  34. S.R. Silva, T.H. Nakagawa, A.L.G. Ferreira, L.C. Garcia, J.E.M. Santos, F.V. Serrão, Lower limb strength and flexibility in athletes with and without patellar tendinopathy. Phys. Ther. Sport. 20, 19–25 (2016)

    Article  Google Scholar 

  35. Fess E.: Grip strength. Clinical assessment recommendations. American Society of Hand Therapists. 41–45. Chicago (1992)

  36. F.L.F. Eichinger, A.V. Soares, J.M. Carvalho, M.S. Gevaerd, S.C. Domenech, N.G. Borges, Dinamometria lombar: Um teste funcional para o tronco. Rev. Bras. Med Trab. 14, 120–126 (2016)

    Article  Google Scholar 

  37. S. Dorsch, L. Ada, C.G. Canning, Lower limb strength is significantly impaired in all muscle groups in ambulatory people with chronic stroke: a cross-sectional study. Arch. Phys. Med. Rehabil. 97, 522–527 (2016)

    Article  PubMed  Google Scholar 

  38. U. Grevstad, P. Jæger, J.K. Sørensen, B. Gottschau, B. Ilfeld, M. Ballegaard, M. Hagelskjaer, J.B. Dahl, The effect of local anesthetic volume within the adductor canal on quadriceps femoris function evaluated by electromyography: a randomized, observer- and infject-blinded, placebo-controlled study in volunteers. Anesth. Analg. 123, 493–500 (2016)

    Article  CAS  PubMed  Google Scholar 

  39. H.J. Hermens, B. Freriks, C. Disselhorst-Klug, G. Rau, Development of recommendations for SEMG sensors and sensor placement procedures. J. Electromyogr. Kinesiol. 10, 361–374 (2000)

    Article  CAS  PubMed  Google Scholar 

  40. D.M. Pincivero, R.C. Green, J.D. Mark, R.M. Campy, Gender and muscle differences in EMG amplitude and median frequency, and variability during maximal voluntary contractions of the quadriceps femoris. J. Electromyogr. Kinesiol. 10, 189–196 (2000)

    Article  CAS  PubMed  Google Scholar 

  41. E.C. Conchola, R.M. Thiele, T.B. Palmer, D.B. Smith, B.J. Thompson, Effects of neuromuscular fatigue on electromechanical delay of the leg extensors and flexors in young men and women. Muscle Nerve 52, 844–851 (2015)

    Article  PubMed  Google Scholar 

  42. M.W. Buckthorpe, R. Hannah, T.G. Pain, J.P. Folland, Reliability of neuromuscular measurements during explosive isometric contractions, with special reference to electromyography normalization techniques. Muscle Nerve 46, 566–576 (2012)

    Article  PubMed  Google Scholar 

  43. M. Beretta-Piccoli, G. D’Antona, M. Barbero, B. Fisher, C.M. Dieli-Conwright, R. Clijsen, C. Cescon, Evaluation of central and peripheral fatigue in the quadriceps using fractal dimension and conduction velocity in young females. PLoS. One. 10, 1–15 (2015)

    Article  CAS  Google Scholar 

  44. E. Hohenauer, C. Cescon, T. Deliens, P. Clarys, R. Clijsen, The effect of local skin cooling before a sustained, submaximal isometric contraction on fatigue and isometric quadriceps femoris performance: a randomized controlled trial. J. Therm. Biol. 65, 88–94 (2017)

    Article  PubMed  Google Scholar 

  45. J.A.S. Barreto-Filho, M.R.S. Alcantara, R. Salvatori, M.A. Barreto, A.C.S. Sousa, V. Bastos, A.H. Souza, R.M.C. Pereira, P.E. Clayton, M.S. Gill, M.H. Aguiar-Oliveira, Familial isolated growth hormone deficiency is associated with increased systolic blood pressure, central obesity and dyslipidemia. J. Clin. Endocrinol. Metab. 87, 2018–2023 (2002)

    Article  CAS  PubMed  Google Scholar 

  46. R.C. Cuneo, F. Salomon, M. Wiles, P.H. Sönksen, Skeletal muscle performance in adults with growth hormone deficiency. Horm. Res. 33, 55–60 (1990)

    Article  PubMed  Google Scholar 

  47. A.R. Hoffman, J.E. Kuntze, J. Baptista, H.B.A. Baum, G.P. Baumann, B.M.K. Biller, R.V. Clark, D. Cook, S.E. Inzucchi, D. Kleinberg, A. Klibanski, L.S. Phillips, E.C. Ridgway, R.J. Robbins, J. Schlechte, M. Sharma, M.O. Thorner, M.L. Vance, Growth hormone (GH) replacement therapy in adult-onset gh deficiency: effects on body composition in men and women in a double-blind, randomized, placebo-controlled trial. J. Clin. Endocrinol. Metab. 89, 2048–2056 (2004)

    Article  CAS  PubMed  Google Scholar 

  48. S. Gonzalez, T. Sathyapalan, Z. Javed, S.L. Atkin, Effects of growth hormone replacement on peripheral muscle and exercise capacity in severe growth hormone deficiency. Front Endocrinol. (Lausanne). 8, 1–7 (2018)

    Google Scholar 

  49. G. Gotherstrom, M. Elbornsson, K. Stibrant-Sunnerhagen, B.A. Bengtsson, G. Johannsson, J. Svensson, Muscle strength in elderly adults with GH deficiency after 10 years of GH replacement. Eur. J. Endocrinol. 163, 207–215 (2010)

    Article  CAS  PubMed  Google Scholar 

  50. W.M. Widdowson, J. Gibney, The effect of growth hormone replacement on exercise capacity in patients with GH deficiency: a metaanalysis. J. Clin. Endocrinol. Metab. 93, 4413–4417 (2008)

    Article  CAS  PubMed  Google Scholar 

  51. R. Borde, T. Hortobágyi, U. Granacher, Dose–response relationships of resistance training in healthy old adults: a systematic review and meta-analysis. Sports Med. 45, 1693–1720 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  52. T.M. Manini, B.C. Clark, Dynapenia and aging: an update. J. Gerontol. A. Biol. Sci. Med. Sci. 67, 28–40 (2012)

    Article  PubMed  Google Scholar 

  53. García-Hermoso A., Cavero-Redondo I., Ramírez-Vélez R., Ruiz J. R., Ortega F. B., Lee D. C., Martínez-Vizcaíno V.: Muscular strength as a predictor of all-cause mortality in an apparently healthy population: a systematic review and meta-analysis of data from approximately 2 million men and women. Arch Phys Med Rehabil. https://doi.org/10.1016/j.apmr.2018.01.008

  54. I.C. Van-Nieuwpoort, M.C. Vlot, L.A. Schaap, P. Lips, M.L. Drent, The relationship between serum IGF-1, handgrip strength, physical performance and falls in elderly men and women. Eur. J. Endocrinol. 179, 73–84 (2018)

    Article  CAS  PubMed  Google Scholar 

  55. M.V. Narici, H. Hoppeler, B. Kayser, L. Landoni, H. Claassen, C. Gavardi, M. Conti, P. Cerretelli, Human quadriceps cross-sectional area, torque and neural activation during 6 months strength training. Acta Physiol. Scand. 157, 175–186 (1996)

    Article  CAS  PubMed  Google Scholar 

  56. C.J. Luca, The use of surface electromyography in biomechanics. J. Appl. Bio. 13, 135–163 (1997)

    Google Scholar 

  57. A. Sinha, K.G. Hollingsworth, S. Ball, T. Cheetham, Impaired quality of life in growth hormone-deficient adults is independent of the altered skeletal muscle oxidative metabolism found in conditions with peripheral fatigue. Clin. Endocrinol. (Oxf.). 80, 107–114 (2014)

    Article  CAS  PubMed  Google Scholar 

  58. E. Shurka, Z. Laron, Adjustment and rehabilitation problems of children and adolescents with growth retardation. I. Familial dwarfism with high plasma immunoreactive human growth hormone. Isr. J. Med. Sci. 11, 352–357 (1975)

    CAS  PubMed  Google Scholar 

  59. Laron Z.: Muscle force and endurance in untreated adult and IGF-I treated children with laron syndrome. In Iaron syndrome - from man to mouse, pp. 161–164. Springer Berlin Heidelberg (2011)

  60. S. Leone, A. Chiavaroli, R. Shohreh, C. Ferrante, A. Ricciuti, F. Manippa, L. Recinella, C.D. Nisio, G. Orlando, R. Salvatori, M. Vacca, L. Brunetti, Increased locomotor and thermogenic activity in mice with targeted ablation of the GHRH gene. Growth Horm. IGF Res. 25, 80–84 (2015)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the Associação do Crescimento Físico e Humano de Itabaianinha, for assistance.

Funding

This work was not supported by public or private funds.

Author information

Authors and Affiliations

  1. Laboratory of Motor Control and Body Balance, Center for Health Science Research, Federal University of Sergipe, 49060-100, Sergipe, Brazil

    Alana L Andrade-Guimarães, Fabiano Alvim-Pereira, Giulliani A. Moreira Brasileiro, Ananda A Santana-Ribeiro, Hugo A. Santos-Carvalho & Miburge B Gois-Junior

  2. Department of Physical Therapy and Post-Graduate Program in Health Science, Federal University of Sergipe, The GREAT Group (GRupo de Estudos em ATividade física), Sergipe, Brazil

    Alana L Andrade-Guimarães, Vitor O. Carvalho, Giulliani A. Moreira Brasileiro & Miburge B Gois-Junior

  3. Division of Endocrinology, Federal University of Sergipe, 49060-100, Aracaju, Sergipe, Brazil

    Manuel H Aguiar-Oliveira & Carla R. P. Oliveira

  4. Division of Endocrinology, Diabetes and Metabolism, The Johns Hopkins University School of Medicine Baltimore, Baltimore, Maryland, 21287, USA

    Roberto Salvatori

  5. Department of Statistic and Actuarial Sciences, Federal University of Sergipe, Aracaju, Sergipe, Brazil

    Carlos R. Araújo Daniel

  6. Department of Physical Therapy and Neuroscience, Wertheims’College of Nursing and Health Science, Florida International University, Florida, USA

    Edgar R Vieira & Miburge B Gois-Junior

Authors
  1. Alana L Andrade-Guimarães
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manuel H Aguiar-Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roberto Salvatori
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vitor O. Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fabiano Alvim-Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carlos R. Araújo Daniel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giulliani A. Moreira Brasileiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ananda A Santana-Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hugo A. Santos-Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Carla R. P. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Edgar R Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Miburge B Gois-Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roberto Salvatori.

Ethics declarations

Ethical approval

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

Conflict of interest

The authors declare that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andrade-Guimarães, A.L., Aguiar-Oliveira, M.H., Salvatori, R. et al. Adult individuals with congenital, untreated, severe isolated growth hormone deficiency have satisfactory muscular function. Endocrine 63, 112–119 (2019). https://doi.org/10.1007/s12020-018-1763-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-018-1763-5

KeyWords

Search

Navigation