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Pituitary

pp 1–17 | Cite as

Neuroendocrine changes after aneurysmal subarachnoid haemorrhage

  • Zuleyha KaracaEmail author
  • Aysa Hacioglu
  • Fahrettin Kelestimur
Article
  • 13 Downloads

Abstract

Introduction

The prevalence of pituitary dysfunction is high following aneurysmal subarachnoid hemorrhage (aSAH) and when occurs it may contribute to residual symptoms of aSAH such as decreased cognition and quality of life. Hypopituitarism following aSAH may have non-specific, subtle symptoms and potentially serious consequences if remained undiagnosed.

Methods

We reviewed the literature on epidemiology, pathophysiology, diagnostic methods and management of neuroendocrine changes after aSAH as well as on the impact of pituitary dysfunction on outcome of the patient.

Results

The prevalence rates of pituitary dysfunction after aSAH varies greatly across studies due to different diagnostic methods, though growth hormone deficiency is generally the most frequently reported followed by adrenocorticotropic hormone, gonadotropin and thyroid stimulating hormone deficiencies. Pituitary deficiency tends to improve over time after aSAH but new onset deficiencies in chronic phase may also occur. There are no clinical parameters to predict the presence of hypopituitarism after aSAH. Age of the patient and surgical procedures are risk factors associated with development of hypopituitarism but the effect of pituitary dysfunction on outcome of the patient is not clear. Replacement of hypocortisolemia and hypothyroidism is essential but treatment of other hormonal insufficiencies should be individualized.

Conclusions

Hypopituitarism following aSAH necessitates screening despite lack of gold standard evaluation tests and cut-off values in the follow up, because missed diagnosis may lead to untoward consequences.

Keywords

Aneurysmal subarachnoid haemorrhage Hypopituitarism Neuroendocrine dysfunction Diabetes insipidus 

Notes

Compliance with ethical standards

Conflict of interest

Zuleyha Karaca, Aysa Hacioglu, Fahrettin Kelestimur declares that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from the only patient whose MR imaging was included in the review.

References

  1. 1.
    van Gijn J, Kerr RS, Rinkel GJ (2007) Subarachnoid haemorrhage. Lancet 369(9558):306–318.  https://doi.org/10.1016/S0140-6736(07)60153-6 Google Scholar
  2. 2.
    Long B, Koyfman A, Runyon MS (2017) Subarachnoid hemorrhage: updates in diagnosis and management. Emerg Med Clin N Am 35(4):803–824.  https://doi.org/10.1016/j.emc.2017.07.001 Google Scholar
  3. 3.
    Tanriverdi F, Ulutabanca H, Unluhizarci K, Selcuklu A, Casanueva FF, Kelestimur F (2008) Three years prospective investigation of anterior pituitary function after traumatic brain injury: a pilot study. Clin Endocrinol (Oxf) 68(4):573–579.  https://doi.org/10.1111/j.1365-2265.2007.03070.x Google Scholar
  4. 4.
    Bendel S, Koivisto T, Ruokonen E, Rinne J, Romppanen J, Vauhkonen I, Kiviniemi V, Uusaro A (2008) Pituitary-adrenal function in patients with acute subarachnoid haemorrhage: a prospective cohort study. Crit Care 12(5):R126.  https://doi.org/10.1186/cc7084 Google Scholar
  5. 5.
    Dimopoulou I, Kouyialis AT, Tzanella M, Armaganidis A, Thalassinos N, Sakas DE, Tsagarakis S (2004) High incidence of neuroendocrine dysfunction in long-term survivors of aneurysmal subarachnoid hemorrhage. Stroke 35(12):2884–2889.  https://doi.org/10.1161/01.STR.0000147716.45571.45 Google Scholar
  6. 6.
    Robba C, Bacigaluppi S, Bragazzi N, Lavinio A, Gurnell M, Bilotta F, Menon DK (2016) Clinical prevalence and outcome impact of pituitary dysfunction after aneurysmal subarachnoid hemorrhage: a systematic review with meta-analysis. Pituitary 19(5):522–535.  https://doi.org/10.1007/s11102-016-0733-2 Google Scholar
  7. 7.
    Hoff WV, Hornabrook RW, Marks V (1961) Hypopituitarism associated with intracranial aneurysms. Br Med J 2(5261):1190–1194Google Scholar
  8. 8.
    Jenkins JS, Buckell M, Carter AB, Westlake S (1969) Hypothalamic-pituitary-adrenal function after subarachnoid haemorrhage. Br Med J 4(5685):707–709Google Scholar
  9. 9.
    Aimaretti G, Ambrosio MR, Di Somma C, Fusco A, Cannavo S, Gasperi M, Scaroni C, De Marinis L, Benvenga S, degli Uberti EC, Lombardi G, Mantero F, Martino E, Giordano G, Ghigo E (2004) Traumatic brain injury and subarachnoid haemorrhage are conditions at high risk for hypopituitarism: screening study at 3 months after the brain injury. Clin Endocrinol (Oxf) 61(3):320–326.  https://doi.org/10.1111/j.1365-2265.2004.02094.x Google Scholar
  10. 10.
    Khajeh L, Blijdorp K, Heijenbrok-Kal MH, Sneekes EM, van den Berg-Emons HJ, van der Lely AJ, Dippel DW, Neggers SJ, Ribbers GM, van Kooten F (2015) Pituitary dysfunction after aneurysmal subarachnoid haemorrhage: course and clinical predictors-the HIPS study. J Neurol Neurosurg Psychiatry 86(8):905–910.  https://doi.org/10.1136/jnnp-2014-307897 Google Scholar
  11. 11.
    Srinivasan L, Roberts B, Bushnik T, Englander J, Spain DA, Steinberg GK, Ren L, Sandel ME, Al-Lawati Z, Teraoka J, Hoffman AR, Katznelson L (2009) The impact of hypopituitarism on function and performance in subjects with recent history of traumatic brain injury and aneurysmal subarachnoid haemorrhage. Brain Inj 23(7):639–648.  https://doi.org/10.1080/02699050902970778 Google Scholar
  12. 12.
    Schneider HJ, Kreitschmann-Andermahr I, Ghigo E, Stalla GK, Agha A (2007) Hypothalamopituitary dysfunction following traumatic brain injury and aneurysmal subarachnoid hemorrhage: a systematic review. JAMA 298(12):1429–1438.  https://doi.org/10.1001/jama.298.12.1429 Google Scholar
  13. 13.
    Kreitschmann-Andermahr I, Hoff C, Saller B, Niggemeier S, Pruemper S, Hutter BO, Rohde V, Gressner A, Matern S, Gilsbach JM (2004) Prevalence of pituitary deficiency in patients after aneurysmal subarachnoid hemorrhage. J Clin Endocrinol Metab 89(10):4986–4992.  https://doi.org/10.1210/jc.2004-0146 Google Scholar
  14. 14.
    Aimaretti G, Ambrosio MR, Di Somma C, Gasperi M, Cannavo S, Scaroni C, Fusco A, Del Monte P, De Menis E, Faustini-Fustini M, Grimaldi F, Logoluso F, Razzore P, Rovere S, Benvenga S, Degli Uberti EC, De Marinis L, Lombardi G, Mantero F, Martino F, Giordano G, Ghigo E (2005) Residual pituitary function after brain injury-induced hypopituitarism: a prospective 12-month study. J Clin Endocrinol Metab 90(11):6085–6092.  https://doi.org/10.1210/jc.2005-0504 Google Scholar
  15. 15.
    Weant KA, Sasaki-Adams D, Dziedzic K, Ewend M (2008) Acute relative adrenal insufficiency after aneurysmal subarachnoid hemorrhage. Neurosurgery 63(4):645–649.  https://doi.org/10.1227/01.NEU.0000325728.50939.15 (discussion 649–650 )Google Scholar
  16. 16.
    Jovanovic V, Pekic S, Stojanovic M, Tasic G, Djurovic B, Soldatovic I, Doknic M, Miljic D, Djurovic M, Medic-Stojanoska M, Popovic V (2010) Neuroendocrine dysfunction in patients recovering from subarachnoid hemorrhage. Hormones (Athens) 9(3):235–244Google Scholar
  17. 17.
    Klose M, Brennum J, Poulsgaard L, Kosteljanetz M, Wagner A, Feldt-Rasmussen U (2010) Hypopituitarism is uncommon after aneurysmal subarachnoid haemorrhage. Clin Endocrinol (Oxf) 73(1):95–101.  https://doi.org/10.1111/j.1365-2265.2010.03791.x Google Scholar
  18. 18.
    Poll EM, Bostrom A, Burgel U, Reinges MH, Hans FJ, Gilsbach JM, Kreitschmann-Andermahr I (2010) Cortisol dynamics in the acute phase of aneurysmal subarachnoid hemorrhage: associations with disease severity and outcome. J Neurotrauma 27(1):189–195.  https://doi.org/10.1089/neu.2009.1014 Google Scholar
  19. 19.
    Lammert A, Bode H, Hammes HP, Birck R, Fatar M, Zohsel K, Braun J, Schmieder K, Diepers M, Schubert GA, Barth M, Thome C, Seiz M (2011) Neuro-endocrine and neuropsychological outcome after aneurysmal subarachnoid hemorrhage (aSAH): a prospective cohort study. Exp Clin Endocrinol Diabetes 119(2):111–116.  https://doi.org/10.1055/s-0030-1262815 Google Scholar
  20. 20.
    Lammert A, Bode H, Hammes HP, Birck R, Fatar M, Zohsel K, Schmieder K, Schubert GA, Thome C, Seiz M (2012) Aneurysmal subarachnoid hemorrhage (aSAH) results in low prevalence of neuro-endocrine dysfunction and NOT deficiency. Pituitary 15(4):505–512.  https://doi.org/10.1007/s11102-011-0357-5 Google Scholar
  21. 21.
    Dutta P, Mukherjee KK, Chaudhary PK, Masoodi SR, Anand S, Pathak A, Shah VN, Mathuriya SN (2012) Pituitary dysfunction in survivors of spontaneous subarachnoid hemorrhage of anterior communicating artery and middle cerebral artery aneurysms: A comparative study. Neurol India 60(4):390–394Google Scholar
  22. 22.
    Karaca Z, Tanriverdi F, Dagli AT, Selcuklu A, Casanueva FF, Unluhizarci K, Kelestimur F (2013) Three years prospective investigation of pituitary functions following subarachnoid haemorrhage. Pituitary 16(1):76–82.  https://doi.org/10.1007/s11102-012-0377-9 Google Scholar
  23. 23.
    Lanterna LA, Spreafico V, Gritti P, Prodam F, Signorelli A, Biroli F, Aimaretti G (2013) Hypocortisolism in noncomatose patients during the acute phase of subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 22(7):e189–e196.  https://doi.org/10.1016/j.jstrokecerebrovasdis.2012.11.002 Google Scholar
  24. 24.
    Pereira JL, Albuquerque LA, Dellaretti M, Carvalho GT, Vieira G Jr, Brochado VM, Drummond AV, Morais JE, Ferreira LM, Miranda PA, Sousa AA (2013) Pituitary deficiency after aneurysmal subarachnoid hemorrhage. Clinics (Sao Paulo) 68(6):745–749.  https://doi.org/10.6061/clinics/2013(06)04 Google Scholar
  25. 25.
    Kopczak A, Kilimann I, von Rosen F, Krewer C, Schneider HJ, Stalla GK, Schneider M (2014) Screening for hypopituitarism in 509 patients with traumatic brain injury or subarachnoid hemorrhage. J Neurotrauma 31(1):99–107.  https://doi.org/10.1089/neu.2013.3002 Google Scholar
  26. 26.
    Kronvall E, Valdemarsson S, Saveland H, Nilsson OG (2014) Pituitary dysfunction after aneurysmal subarachnoid hemorrhage is associated with impaired early outcome. World Neurosurg 81(3–4):529–537.  https://doi.org/10.1016/j.wneu.2013.10.038 Google Scholar
  27. 27.
    Kronvall E, Valdemarsson S, Saveland H, Nilsson OG (2015) High prevalence of pituitary dysfunction after aneurysmal subarachnoid hemorrhage: a long-term prospective study using dynamic endocrine testing. World Neurosurg 83(4):574–582.  https://doi.org/10.1016/j.wneu.2014.12.007 Google Scholar
  28. 28.
    Kronvall E, Sonesson B, Valdemarsson S, Siemund R, Saveland H, Nilsson OG (2016) Reduced quality of life in patients with pituitary dysfunction after aneurysmal subarachnoid hemorrhage: a prospective longitudinal study. World Neurosurg 88:83–91.  https://doi.org/10.1016/j.wneu.2015.12.057 Google Scholar
  29. 29.
    Goto Y, Oshino S, Nishino A, Fujinaka T, Nakamura H, Yuguchi T, Mori S, Yoshimine T, Saitoh Y (2016) Pituitary dysfunction after aneurysmal subarachnoid hemorrhage in Japanese patients. J Clin Neurosci 34:198–201.  https://doi.org/10.1016/j.jocn.2016.07.003 Google Scholar
  30. 30.
    Krewer C, Schneider M, Schneider HJ, Kreitschmann-Andermahr I, Buchfelder M, Faust M, Berg C, Wallaschofski H, Renner C, Uhl E, Koenig E, Jordan M, Stalla GK, Kopczak A (2016) Neuroendocrine disturbances one to five or more years after traumatic brain injury and aneurysmal subarachnoid hemorrhage: data from the German database on hypopituitarism. J Neurotrauma 33(16):1544–1553.  https://doi.org/10.1089/neu.2015.4109 Google Scholar
  31. 31.
    Vieira G Jr, de Albuquerque LA, de Avellar AB, Pereira JL, Dellaretti M, Miranda PA, Macedo RA, da Silva LA, Gusmao SN (2016) Long-term follow-up of anterior pituitary deficiency after aneurysmal subarachnoid hemorrhage: prospective cohort. J Stroke Cerebrovasc Dis 25(10):2405–2414.  https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.06.011 Google Scholar
  32. 32.
    Giritharan S, Cox J, Heal CJ, Hughes D, Gnanalingham K, Kearney T (2017) The prevalence of growth hormone deficiency in survivors of subarachnoid haemorrhage: results from a large single centre study. Pituitary 20(6):624–634.  https://doi.org/10.1007/s11102-017-0825-7 Google Scholar
  33. 33.
    Can A, Gross BA, Smith TR, Dammers R, Dirven CM, Woodmansee WW, Laws ER, Du R (2016) Pituitary dysfunction after aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Neurosurgery 79(2):253–264.  https://doi.org/10.1227/NEU.0000000000001157 Google Scholar
  34. 34.
    Khajeh L, Blijdorp K, Neggers SJ, Ribbers GM, Dippel DW, van Kooten F (2014) Hypopituitarism after subarachnoid haemorrhage, do we know enough? BMC Neurol 14:205.  https://doi.org/10.1186/s12883-014-0205-0 Google Scholar
  35. 35.
    Hannon MJ, Behan LA, O’Brien MM, Tormey W, Javadpour M, Sherlock M, Thompson CJ (2015) Chronic hypopituitarism is uncommon in survivors of aneurysmal subarachnoid haemorrhage. Clin Endocrinol (Oxf) 82(1):115–121.  https://doi.org/10.1111/cen.12533 Google Scholar
  36. 36.
    Kreitschmann-Andermahr I, Hartmann Y, Poll E, Schneider HJ, Buchfelder M, Stalla GK (2011) The German database on hypopituitarism after traumatic brain injury and aneurysmal subarachnoid hemorrhage - description, objectives and design. Exp Clin Endocrinol Diabetes 119(1):15–20.  https://doi.org/10.1055/s-0030-1253414 Google Scholar
  37. 37.
    Gardner CJ, Javadpour M, Stoneley C, Purthuran M, Biswas S, Daousi C, MacFarlane IA, Cuthbertson DJ (2013) Low prevalence of hypopituitarism after subarachnoid haemorrhage using confirmatory testing and with BMI-specific GH cut-off levels. Eur J Endocrinol 168(4):473–481.  https://doi.org/10.1530/EJE-12-0849 Google Scholar
  38. 38.
    Tanriverdi F, Schneider HJ, Aimaretti G, Masel BE, Casanueva FF, Kelestimur F (2015) Pituitary dysfunction after traumatic brain injury: a clinical and pathophysiological approach. Endocr Rev 36(3):305–342.  https://doi.org/10.1210/er.2014-1065 Google Scholar
  39. 39.
    Karaca Z, Tanriverdi F, Unluhizarci K, Kelestimur F (2016) GH and pituitary hormone alterations after traumatic brain injury. Prog Mol Biol Transl Sci 138:167–191.  https://doi.org/10.1016/bs.pmbts.2015.10.010 Google Scholar
  40. 40.
    Crompton MR (1963) Hypothalamic lesions following the rupture of cerebral berry aneurysms. Brain 86:301–314Google Scholar
  41. 41.
    Sercombe R, Sercombe C, Oudart N, Seylaz J (2002) Critical role of endothelial nitric oxide synthase and cyclooxygenase in response of rabbit basilar artery to serotonin. Jpn J Pharmacol 90(1):67–76Google Scholar
  42. 42.
    Ioachimescu AG, Barrow DL (2015) Subarachnoid Hemorrhage and the Pituitary. World Neurosurg 83(6):1026–1028.  https://doi.org/10.1016/j.wneu.2015.01.044 Google Scholar
  43. 43.
    Vespa P, Participants in the International Multi-Disciplinary Consensus Conference on the Critical Care Management of Subarachnoid, H.: SAH pituitary adrenal dysfunction. Neurocrit Care 15(2), 365–368 (2011).  https://doi.org/10.1007/s12028-011-9595-7
  44. 44.
    Khajeh L, Ribbers GM, Heijenbrok-Kal MH, Blijdorp K, Dippel DW, Sneekes EM, van den Berg-Emons HJ, van der Lely AJ, Neggers SJ, van Kooten F (2016) The effect of hypopituitarism on fatigue after subarachnoid hemorrhage. Eur J Neurol 23(8):1269–1274.  https://doi.org/10.1111/ene.13014 Google Scholar
  45. 45.
    Kreitschmann-Andermahr I, Poll E, Hutter BO, Reineke A, Kristes S, Gilsbach JM, Saller B (2007) Quality of life and psychiatric sequelae following aneurysmal subarachnoid haemorrhage: does neuroendocrine dysfunction play a role? Clin Endocrinol (Oxf) 66(6):833–837.  https://doi.org/10.1111/j.1365-2265.2007.02821.x Google Scholar
  46. 46.
    Karamouzis I, Pagano L, Prodam F, Mele C, Zavattaro M, Busti A, Marzullo P, Aimaretti G (2016) Clinical and diagnostic approach to patients with hypopituitarism due to traumatic brain injury (TBI), subarachnoid hemorrhage (SAH), and ischemic stroke (IS). Endocrine 52(3):441–450.  https://doi.org/10.1007/s12020-015-0796-2 Google Scholar
  47. 47.
    Cohan P, Wang C, McArthur DL, Cook SW, Dusick JR, Armin B, Swerdloff R, Vespa P, Muizelaar JP, Cryer HG, Christenson PD, Kelly DF (2005) Acute secondary adrenal insufficiency after traumatic brain injury: a prospective study. Crit Care Med 33(10):2358–2366Google Scholar
  48. 48.
    Brandt L, Saveland H, Valdemarsson S, Sjoholm H, Reinstrup P (2004) Fatigue after aneurysmal subarachnoid hemorrhage evaluated by pituitary function and 3D-CBF. Acta Neurol Scand 109(2):91–96Google Scholar
  49. 49.
    Karaca Z, Lale A, Tanriverdi F, Kula M, Unluhizarci K, Kelestimur F (2011) The comparison of low and standard dose ACTH and glucagon stimulation tests in the evaluation of hypothalamo-pituitary-adrenal axis in healthy adults. Pituitary 14(2):134–140.  https://doi.org/10.1007/s11102-010-0270-3 Google Scholar
  50. 50.
    Simsek Y, Karaca Z, Tanriverdi F, Unluhizarci K, Selcuklu A, Kelestimur F (2015) A comparison of low-dose ACTH, glucagon stimulation and insulin tolerance test in patients with pituitary disorders. Clin Endocrinol (Oxf) 82(1):45–52.  https://doi.org/10.1111/cen.12528 Google Scholar
  51. 51.
    Cho HY, Kim JH, Kim SW, Shin CS, Park KS, Kim SW, Jang HC, Kim SY (2014) Different cut-off values of the insulin tolerance test, the high-dose short Synacthen test (250 mug) and the low-dose short Synacthen test (1 mug) in assessing central adrenal insufficiency. Clin Endocrinol (Oxf) 81(1):77–84.  https://doi.org/10.1111/cen.12397 Google Scholar
  52. 52.
    Berg C, Meinel T, Lahner H, Yuece A, Mann K, Petersenn S (2010) Diagnostic utility of the glucagon stimulation test in comparison to the insulin tolerance test in patients following pituitary surgery. Eur J Endocrinol 162(3):477–482.  https://doi.org/10.1530/EJE-09-0824 Google Scholar
  53. 53.
    Qureshi AI, Suri MF, Sung GY, Straw RN, Yahia AM, Saad M, Guterman LR, Hopkins LN (2002) Prognostic significance of hypernatremia and hyponatremia among patients with aneurysmal subarachnoid hemorrhage. Neurosurgery 50(4):749–755 (discussion 755–746)Google Scholar
  54. 54.
    Robertson GL, Aycinena P, Zerbe RL (1982) Neurogenic disorders of osmoregulation. Am J Med 72(2):339–353Google Scholar
  55. 55.
    McIver B, Connacher A, Whittle I, Baylis P, Thompson C (1991) Adipsic hypothalamic diabetes insipidus after clipping of anterior communicating artery aneurysm. BMJ 303(6815):1465–1467Google Scholar
  56. 56.
    Crowley RK, Sherlock M, Agha A, Smith D, Thompson CJ (2007) Clinical insights into adipsic diabetes insipidus: a large case series. Clin Endocrinol (Oxf) 66(4):475–482.  https://doi.org/10.1111/j.1365-2265.2007.02754.x Google Scholar
  57. 57.
    Eisenberg Y, Frohman LA (2016) Adipsic diabetes insipidus: a review. Endocr Pract 22(1):76–83.  https://doi.org/10.4158/EP15940.RA Google Scholar
  58. 58.
    Hannon MJ, Sherlock M, Thompson CJ (2011) Pituitary dysfunction following traumatic brain injury or subarachnoid haemorrhage—in “endocrine management in the intensive care unit”. Best Pract Res Clin Endocrinol Metab 25(5):783–798.  https://doi.org/10.1016/j.beem.2011.06.001 Google Scholar
  59. 59.
    Garrahy A, Sherlock M, Thompson CJ (2017) MANAGEMENT OF ENDOCRINE DISEASE: neuroendocrine surveillance and management of neurosurgical patients. Eur J Endocrinol 176(5):R217–R233.  https://doi.org/10.1530/EJE-16-0962 Google Scholar
  60. 60.
    Chen I, Mitchell P (2016) Serum potassium and sodium levels after subarachnoid haemorrhage. Br J Neurosurg 30(5):554–559.  https://doi.org/10.1080/02688697.2016.1181151 Google Scholar
  61. 61.
    Sherlock M, O’Sullivan E, Agha A, Behan LA, Rawluk D, Brennan P, Tormey W, Thompson CJ (2006) The incidence and pathophysiology of hyponatraemia after subarachnoid haemorrhage. Clin Endocrinol (Oxf) 64(3):250–254.  https://doi.org/10.1111/j.1365-2265.2006.02432.x Google Scholar
  62. 62.
    Hannon MJ, Behan LA, O’Brien MM, Tormey W, Ball SG, Javadpour M, Sherlock M, Thompson CJ (2014) Hyponatremia following mild/moderate subarachnoid hemorrhage is due to SIAD and glucocorticoid deficiency and not cerebral salt wasting. J Clin Endocrinol Metab 99(1):291–298.  https://doi.org/10.1210/jc.2013-3032 Google Scholar
  63. 63.
    See AP, Wu KC, Lai PM, Gross BA, Du R (2016) Risk factors for hyponatremia in aneurysmal subarachnoid hemorrhage. J Clin Neurosci 32:115–118.  https://doi.org/10.1016/j.jocn.2016.04.006 Google Scholar
  64. 64.
    Alimohamadi M, Saghafinia M, Alikhani F, Danial Z, Shirani M, Amirjamshidi A (2016) Impact of electrolyte imbalances on the outcome of aneurysmal subarachnoid hemorrhage: A prospective study. Asian J Neurosurg 11(1):29–33.  https://doi.org/10.4103/1793-5482.154978 Google Scholar
  65. 65.
    Mapa B, Taylor BE, Appelboom G, Bruce EM, Claassen J, Connolly ES Jr (2016) Impact of hyponatremia on morbidity, mortality, and complications after aneurysmal subarachnoid hemorrhage: a systematic review. World Neurosurg 85:305–314.  https://doi.org/10.1016/j.wneu.2015.08.054 Google Scholar
  66. 66.
    Greenberg JK, Washington CW, Guniganti R, Dacey RG Jr, Derdeyn CP, Zipfel GJ (2016) Causes of 30-day readmission after aneurysmal subarachnoid hemorrhage. J Neurosurg 124(3):743–749.  https://doi.org/10.3171/2015.2.JNS142771 Google Scholar
  67. 67.
    Mistry AM, Mistry EA, Ganesh Kumar N, Froehler MT, Fusco MR, Chitale RV (2016) Corticosteroids in the management of hyponatremia, hypovolemia, and vasospasm in subarachnoid hemorrhage: a meta-analysis. Cerebrovasc Dis 42(3–4):263–271.  https://doi.org/10.1159/000446251 Google Scholar
  68. 68.
    Verbalis JG, Goldsmith SR, Greenberg A, Korzelius C, Schrier RW, Sterns RH, Thompson CJ (2013) Diagnosis, evaluation, and treatment of hyponatremia: expert panel recommendations. Am J Med 126(10 Suppl 1):S1–S42.  https://doi.org/10.1016/j.amjmed.2013.07.006 Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Endocrinology and MetabolismErciyes University Medical SchoolKayseriTurkey
  2. 2.Department of Endocrinology and MetabolismYeditepe University Medical SchoolIstanbulTurkey

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