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Year 2019, Volume: 13 Issue: 3, 155 - 162, 31.12.2019

Abstract

References

  • 1. Kalsbeek A, Fliers E, Franke AN, Wortel J, Buijs RM. Functional connections between the suprachiasmatic nucleus and the thyroid gland as revealed by lesioning and viral tracing techniques in the rat. Endocrinology 2000;141:3832–41. 2. Sundler F, Grunditz T, Håkanson R, Uddman R. Innervation of the thyroid. A study of the rat using retrograde tracing and immunocytochemistry. Acta Histochem Suppl 1989;37:191–8. 3. Melander A. Aminergic regulation of thyroid activity: importance of the sympathetic innervation and of the mast cells of the thyroid gland. Acta Med Scand 1977;201:257–62. 4. Onen MR, Yilmaz I, Ramazanoglu L, Aydin MD, Keles S, Baykal O, Aydin N, Gundogdu C. Uncovering the forgotten effect of superior cervical ganglia on pupil diameter in subarachnoid hemorrhage: an experimental study. Turk Neurosurg 2018;28:48–55. 5. Melander A, Sundler F, Westgren U. Sympathetic innervation of the thyroid: variation with species and with age. Endocrinology 1975;96: 102–6. 6. Diamantis E, Farmaki P, Savvanis S, Athanasiadis G, Troupis T, Damaskos C. Symphathetic nerve injury in thyroid cancer. Acta Medica (Hradec Králové) 2017;60:135–9. 7. Baryla J, Greniuk G, Lakomy M. The adrenergic and cholinergic innervation of the thyroid chicken gland. Folia Morphol (Warsz) 2003;62:247–9. 8. Van Sande J, Dumont JE, Melander A, Sundler F. Presence and influence of cholinergic nerves in the human thyroid. J Clin Endocrinol Metab 1980;51:500–2. 9. Ito H, Matsuda K, Sato A, Tohgi H. Cholinergic and VIPergic vasodilator actions of parasympathetic nerves on the thyroid blood flow in rats. Jpn J Physiol 1987;37:1005–17. 10. Stern JE, Sarmiento MI, Cardinali DP. Parasympathetic control of parathyroid hormone and calcitonin secretion in rats. J Auton Nerv Syst 1994;48:45–53. 11. Grunditz T, Ekman R, Håkanson R, Rerup C, Sundler F, Uddman R. Calcitonin gene-related peptide in thyroid nerve fibers and C cells: effects on thyroid hormone secretion and response to hypercalcemia. Endocrinology 1986;119:2313–24. 12. Jallageas M, Mas N, Saboureau M, Roussel JP, Lacroix A. Effects of bilateral superior cervical ganglionectomy on thyroid and gonadal functions in the edible dormouse Glis glis. Comp Biochem Physiol Comp Physiol 1993;104:299–304. 13. Young JB, Bürgi-Saville ME, Bürgi U, Landsberg L. Sympathetic nervous system activity in rat thyroid: potential role in goitrogenesis. Am J Physiol Endocrinol Metab 2005;288:E861–7. 14. Flett DL, Bell C. Topography of functional subpopulations of neurons in the superior cervical ganglion of the rat. J Anat 1991;177:55– 66. 15. Boado RJ, Romeo HE, Chuluyan HE, Cageao L, Cardinali DP, Zaninovich AA. Evidence suggesting that the sympathetic nervous system mediates thyroidal depression in turpentine-induced nonthyroidal illness syndrome. Neuroendocrinology 1991;53:360–4. 16. Romeo HE, González Solveyra C, Vacas MI, Rosenstein RE, Barontini M, Cardinali DP. Origins of the sympathetic projections to rat thyroid and parathyroid glands. J Auton Nerv Syst 1986;17:63– 70. 17. Cardinali DP, Vacas MI, Gejman PV, Pisarev MA, Barontini M, Boado RJ, Juvenal GJ. The sympathetic superior cervical ganglia as “little neuroendocrine brains”. Acta Physiol Lat Am 1983;33:205–21. 18. de Rooij NK, Linn FHH, Van der Plas JA, Algra B, Rinkel GJE. Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends. J Neurol Neurosurg Psychiatry 2007;78:1365–72. 19. Dirnagl U, Macleod MR. Stroke research at a road block: The streets from adversity should be paved with meta-analysis and good laboratory practice. Br J Pharmacol 2009;157:1154–6. 20. Marbacher S, Grüter B, Schöpf S, Croci D, Nevzati E, D’Alonzo D, Lattmann J, Roth T, Bircher B, Wolfert C, Muroi C, Dutilh G, Widmer HR, Fandino J. Systematic review of in vivo animal models of subarachnoid hemorrhage: species, standard parameters, and outcomes. Translat Stroke Res 2019;10:250–8. 21. Chan RC, Durity FA, Thompson GB, Nugent RA, Kendall M. The role of the prostacyclin-thromboxane system in cerebral vasospasm following induced subarachnoid hemorrhage in the rabbit. J Neurosurg 1984;61:1120–8. 22. Wilkins RH. Cerebral vasospasm. Crit Rev Neurobiol 1990;6:51– 77. 23. Silva JE, Bianco SD. Thyroid-adrenergic interactions: physiological and clinical implications. Thyroid 2008;18:157–65. 24. Zerek-Melen G, Lewinski A. Influence of sympathetic denervation of the thyroid by superior cervical ganglionectomy on the growth processes in the gland in basal conditions and after hemithyroidectomy. Acta Physiol Pharmacol Latinoam 1988;38:377–87. 25. Cardinali DP, Vacas MI, Gejman PV. The sympathetic superior cervical ganglia as peripheral neuroendocrine centers. J Neural Transm 1981;52:1–21. 26. Lychkova AE. Nervous regulation of thyroid function.Vestn Ross Akad Med Nauk 2013;6:49–55. 27. Cardinali DP, Sartorio GC, Ladizesky MG, Guillén CE, Soto RJ. Changes in calcitonin release during sympathetic nerve degeneration after superior cervical ganglionectomy of rats. Neuroendocrinology 1986;43:498–503. 28. Edvinsson L, Ekman R, Jansen I, McCulloch J, Mortensen A, Uddman R. Reduced levels of calcitonin gene-related peptide-like immunoreactivity in human brain vessels after subarachnoid haemorrhage. Neurosci Lett 1991;121:151–4. 29. Kokkoris S, Andrews P, Webb DJ. Role of calcitonin gene-related peptide in cerebral vasospasm, and as a therapeutic approach to subarachnoid hemorrhage. Front Endocrinol (Lausanne) 2012;3:135.

The underestimated role of a somatosensory neural network on thyroid gland morphology: an experimental subarachnoid hemorrhage model study

Year 2019, Volume: 13 Issue: 3, 155 - 162, 31.12.2019

Abstract

Objectives: Innervation of the thyroid gland has been attributed to the autonomic nervous system. Although peripheral sympathetic
and parasympathetic innervations of the thyroid gland are well known, little is known about the somatosensory innervation
of the thyroid gland. In this study, alterations on the somatosensory neural network of the thyroid gland following an
experimental subarachnoid hemorrhage were investigated in rabbits.

Methods: Experiments were conducted on 23 rabbits under no medical intervention. Five rabbits were used as control group.
Five rabbits were used as the sham group and serum physiologic (SF) was injected into their cisterna magna. The remaining 13
animals were used as the subarachnoid hemorrhage (SAH) group; their own blood (1 ml) was re-injected into the cisterna magna.
Thyroid hormone levels of animals were measured at the end of one month. Then, histological sections of the middle parts of
the thyroid glands were stained with haematoxylin-eosin (H&E) for investigation of SAH-related damage. The total follicle volume
(TFV) per cubic millimeter of the thyroid gland was estimated by stereological methods. Comparison of degenerated neuronal
density (DND) in the C4 dorsal root ganglia (DRG) was examined bilaterally using H&E and TUNEL stainings.

Results: Following SAH, neuronal degeneration in the cervical DRG caused somatic innervation deficiency, follicular atrophy and
thyroid hormone depletion in the thyroid gland. T3 and T4 hormone levels of the SAH group (T3: 61±8 μg/dl; T4: 1.01±0.12
μg/dl) were significantly (p<0.005) lower than those of control (T3; 103±6 μg/dl, T4: 1.37±0.36 μg/dl) and sham (T3; 94±10
μg/dl; T4: 1.24±0.87 μg/dl) groups. In control groups, mean TFV was 41% / mm3 and DND of C4 DRG was 6±2 / mm3. These
values were significantly lower than those in sham (TFV: 35%/mm3 and DND: 22±7/mm3) and experimental SAH (TFV: 23%/mm3
and DND: 253±49/mm3) groups (p<0.0005 and p<0.0001, respectively).

Conclusion: Thyroid follicle growth and its secretory activity are under the control of a quite complex, multi-originated, yet
incompletely understood innervation pattern. We propose the presence of an underestimated role of a somatosensory neural
network - an interganglionary link between the superior cervical, thyroid, laryngeal, nodose, trigeminal and dorsal root ganglia
- on thyroid gland morphology.

References

  • 1. Kalsbeek A, Fliers E, Franke AN, Wortel J, Buijs RM. Functional connections between the suprachiasmatic nucleus and the thyroid gland as revealed by lesioning and viral tracing techniques in the rat. Endocrinology 2000;141:3832–41. 2. Sundler F, Grunditz T, Håkanson R, Uddman R. Innervation of the thyroid. A study of the rat using retrograde tracing and immunocytochemistry. Acta Histochem Suppl 1989;37:191–8. 3. Melander A. Aminergic regulation of thyroid activity: importance of the sympathetic innervation and of the mast cells of the thyroid gland. Acta Med Scand 1977;201:257–62. 4. Onen MR, Yilmaz I, Ramazanoglu L, Aydin MD, Keles S, Baykal O, Aydin N, Gundogdu C. Uncovering the forgotten effect of superior cervical ganglia on pupil diameter in subarachnoid hemorrhage: an experimental study. Turk Neurosurg 2018;28:48–55. 5. Melander A, Sundler F, Westgren U. Sympathetic innervation of the thyroid: variation with species and with age. Endocrinology 1975;96: 102–6. 6. Diamantis E, Farmaki P, Savvanis S, Athanasiadis G, Troupis T, Damaskos C. Symphathetic nerve injury in thyroid cancer. Acta Medica (Hradec Králové) 2017;60:135–9. 7. Baryla J, Greniuk G, Lakomy M. The adrenergic and cholinergic innervation of the thyroid chicken gland. Folia Morphol (Warsz) 2003;62:247–9. 8. Van Sande J, Dumont JE, Melander A, Sundler F. Presence and influence of cholinergic nerves in the human thyroid. J Clin Endocrinol Metab 1980;51:500–2. 9. Ito H, Matsuda K, Sato A, Tohgi H. Cholinergic and VIPergic vasodilator actions of parasympathetic nerves on the thyroid blood flow in rats. Jpn J Physiol 1987;37:1005–17. 10. Stern JE, Sarmiento MI, Cardinali DP. Parasympathetic control of parathyroid hormone and calcitonin secretion in rats. J Auton Nerv Syst 1994;48:45–53. 11. Grunditz T, Ekman R, Håkanson R, Rerup C, Sundler F, Uddman R. Calcitonin gene-related peptide in thyroid nerve fibers and C cells: effects on thyroid hormone secretion and response to hypercalcemia. Endocrinology 1986;119:2313–24. 12. Jallageas M, Mas N, Saboureau M, Roussel JP, Lacroix A. Effects of bilateral superior cervical ganglionectomy on thyroid and gonadal functions in the edible dormouse Glis glis. Comp Biochem Physiol Comp Physiol 1993;104:299–304. 13. Young JB, Bürgi-Saville ME, Bürgi U, Landsberg L. Sympathetic nervous system activity in rat thyroid: potential role in goitrogenesis. Am J Physiol Endocrinol Metab 2005;288:E861–7. 14. Flett DL, Bell C. Topography of functional subpopulations of neurons in the superior cervical ganglion of the rat. J Anat 1991;177:55– 66. 15. Boado RJ, Romeo HE, Chuluyan HE, Cageao L, Cardinali DP, Zaninovich AA. Evidence suggesting that the sympathetic nervous system mediates thyroidal depression in turpentine-induced nonthyroidal illness syndrome. Neuroendocrinology 1991;53:360–4. 16. Romeo HE, González Solveyra C, Vacas MI, Rosenstein RE, Barontini M, Cardinali DP. Origins of the sympathetic projections to rat thyroid and parathyroid glands. J Auton Nerv Syst 1986;17:63– 70. 17. Cardinali DP, Vacas MI, Gejman PV, Pisarev MA, Barontini M, Boado RJ, Juvenal GJ. The sympathetic superior cervical ganglia as “little neuroendocrine brains”. Acta Physiol Lat Am 1983;33:205–21. 18. de Rooij NK, Linn FHH, Van der Plas JA, Algra B, Rinkel GJE. Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends. J Neurol Neurosurg Psychiatry 2007;78:1365–72. 19. Dirnagl U, Macleod MR. Stroke research at a road block: The streets from adversity should be paved with meta-analysis and good laboratory practice. Br J Pharmacol 2009;157:1154–6. 20. Marbacher S, Grüter B, Schöpf S, Croci D, Nevzati E, D’Alonzo D, Lattmann J, Roth T, Bircher B, Wolfert C, Muroi C, Dutilh G, Widmer HR, Fandino J. Systematic review of in vivo animal models of subarachnoid hemorrhage: species, standard parameters, and outcomes. Translat Stroke Res 2019;10:250–8. 21. Chan RC, Durity FA, Thompson GB, Nugent RA, Kendall M. The role of the prostacyclin-thromboxane system in cerebral vasospasm following induced subarachnoid hemorrhage in the rabbit. J Neurosurg 1984;61:1120–8. 22. Wilkins RH. Cerebral vasospasm. Crit Rev Neurobiol 1990;6:51– 77. 23. Silva JE, Bianco SD. Thyroid-adrenergic interactions: physiological and clinical implications. Thyroid 2008;18:157–65. 24. Zerek-Melen G, Lewinski A. Influence of sympathetic denervation of the thyroid by superior cervical ganglionectomy on the growth processes in the gland in basal conditions and after hemithyroidectomy. Acta Physiol Pharmacol Latinoam 1988;38:377–87. 25. Cardinali DP, Vacas MI, Gejman PV. The sympathetic superior cervical ganglia as peripheral neuroendocrine centers. J Neural Transm 1981;52:1–21. 26. Lychkova AE. Nervous regulation of thyroid function.Vestn Ross Akad Med Nauk 2013;6:49–55. 27. Cardinali DP, Sartorio GC, Ladizesky MG, Guillén CE, Soto RJ. Changes in calcitonin release during sympathetic nerve degeneration after superior cervical ganglionectomy of rats. Neuroendocrinology 1986;43:498–503. 28. Edvinsson L, Ekman R, Jansen I, McCulloch J, Mortensen A, Uddman R. Reduced levels of calcitonin gene-related peptide-like immunoreactivity in human brain vessels after subarachnoid haemorrhage. Neurosci Lett 1991;121:151–4. 29. Kokkoris S, Andrews P, Webb DJ. Role of calcitonin gene-related peptide in cerebral vasospasm, and as a therapeutic approach to subarachnoid hemorrhage. Front Endocrinol (Lausanne) 2012;3:135.
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Details

Primary Language English
Subjects Health Care Administration
Journal Section Original Articles
Authors

Cengiz Öztürk This is me

Mehmet Nuri Koçak This is me

Tuba Demirci This is me

İsmail Malkoç

Mehmet Dumlu Aydın This is me

Publication Date December 31, 2019
Published in Issue Year 2019 Volume: 13 Issue: 3

Cite

APA Öztürk, C., Koçak, M. N., Demirci, T., Malkoç, İ., et al. (2019). The underestimated role of a somatosensory neural network on thyroid gland morphology: an experimental subarachnoid hemorrhage model study. Anatomy, 13(3), 155-162.
AMA Öztürk C, Koçak MN, Demirci T, Malkoç İ, Aydın MD. The underestimated role of a somatosensory neural network on thyroid gland morphology: an experimental subarachnoid hemorrhage model study. Anatomy. December 2019;13(3):155-162.
Chicago Öztürk, Cengiz, Mehmet Nuri Koçak, Tuba Demirci, İsmail Malkoç, and Mehmet Dumlu Aydın. “The Underestimated Role of a Somatosensory Neural Network on Thyroid Gland Morphology: An Experimental Subarachnoid Hemorrhage Model Study”. Anatomy 13, no. 3 (December 2019): 155-62.
EndNote Öztürk C, Koçak MN, Demirci T, Malkoç İ, Aydın MD (December 1, 2019) The underestimated role of a somatosensory neural network on thyroid gland morphology: an experimental subarachnoid hemorrhage model study. Anatomy 13 3 155–162.
IEEE C. Öztürk, M. N. Koçak, T. Demirci, İ. Malkoç, and M. D. Aydın, “The underestimated role of a somatosensory neural network on thyroid gland morphology: an experimental subarachnoid hemorrhage model study”, Anatomy, vol. 13, no. 3, pp. 155–162, 2019.
ISNAD Öztürk, Cengiz et al. “The Underestimated Role of a Somatosensory Neural Network on Thyroid Gland Morphology: An Experimental Subarachnoid Hemorrhage Model Study”. Anatomy 13/3 (December 2019), 155-162.
JAMA Öztürk C, Koçak MN, Demirci T, Malkoç İ, Aydın MD. The underestimated role of a somatosensory neural network on thyroid gland morphology: an experimental subarachnoid hemorrhage model study. Anatomy. 2019;13:155–162.
MLA Öztürk, Cengiz et al. “The Underestimated Role of a Somatosensory Neural Network on Thyroid Gland Morphology: An Experimental Subarachnoid Hemorrhage Model Study”. Anatomy, vol. 13, no. 3, 2019, pp. 155-62.
Vancouver Öztürk C, Koçak MN, Demirci T, Malkoç İ, Aydın MD. The underestimated role of a somatosensory neural network on thyroid gland morphology: an experimental subarachnoid hemorrhage model study. Anatomy. 2019;13(3):155-62.

Anatomy is the official journal of Turkish Society of Anatomy and Clinical Anatomy (TSACA).