Abstract
Background
Guillain-Barré syndrome (GBS), an acquired immune-mediated inflammatory disorder affecting the peripheral nervous system (PNS), is usually complicated with autoimmune diseases including thyroid diseases. Herein, we explored roles of thyroid function and thyroid autoantibodies in the disease severity and its short-term prognosis of GBS. In addition, we further investigated the predictive value of thyroid function for GBS respiratory insufficiency.
Materials and methods
We retrospectively analyzed the clinical data of 219 GBS patients. According to the thyroid function, the enrolled subjects were divided into 2 groups, that is, patients with abnormal thyroid function (case group) and those with normal thyroid function (control group). The clinical characteristics, disease severity, and short-term prognosis of the patients in 2 groups were compared. In addition, we also divided the 219 GBS patients into mechanical ventilation (MV) group and non-MV group according to whether MV was performed within 1 week after admission. The clinical characteristics, disease severity, short-term prognosis, Erasmus GBS respiratory insufficiency score (EGRIS), and the thyroid function were compared in the two groups.
Results
We found that GBS patients with abnormal thyroid function had longer duration of hospitalization, higher frequency of cranial nerve damage, and higher incidence of weakened tendon reflexes. Medical Research Council (MRC) scores on admission, at nadir, and at discharge were lower, and Hughes Functional Grading Scale (HFGS) scores on admission and at discharge were higher in GBS patients with abnormal thyroid function group. More patients in the abnormal thyroid function group had myelin, axonal, and myelin-axonal injuries. In the MV group, the time from onset to admission, MRC scores on admission, and the levels of free triiodothyronine (FT3) were lower; the levels of thyroglobulin antibody (TgAb) and EGRIS were significantly higher than those in the non-MV group. The combination of EGRIS and FT3 serum levels to predict GBS patients with MV, the area under the curve (AUC) was 0.905 (95% CI: 0.861 to 0.948, P < 0.05), sensitivity was 88.9%, and specificity was 84.7%.
Conclusion
Our results suggest that the serum FT3 levels are negatively correlated with disease severity; the serum FT3 might be a biomarker for the incidence and severity of GBS. Both EGRIS and serum FT3 have a predictive value for the occurrence of acute respiratory insufficiency in GBS patients, and the combination of these two indicators can more accurately predict the risk of acute respiratory insufficiency in GBS patients.
Similar content being viewed by others
Abbreviations
- GBS:
-
Guillain-Barré syndrome
- FT3:
-
Free triiodothyronine
- FT4:
-
Free thyroxine
- TSH:
-
Thyroid-stimulating hormone
- TPOAb:
-
Thyroperoxidase antibody
- TgAb:
-
Thyroglobulin antibody
- TH:
-
Thyroid hormone
- PNS:
-
Peripheral nervous system
- MV:
-
Mechanical ventilation
- EGRIS:
-
Erasmus GBS respiratory insufficiency score
- MRC:
-
Medical Research Council
- HFGS:
-
Hughes Functional Grading Scale
- CNS:
-
Central nervous system
- OPCs:
-
Oligodendrocyte precursor cells
- MS:
-
Multiple sclerosis
- CIDP:
-
Chronic inflammatory demyelinating polyneuropathy
- IFN-γ:
-
Interferon γ
- TNF-α:
-
Tumor necrosis factor α
- IL-17:
-
Interleukin-17
- ROS:
-
Reactive oxygen species
- ROC:
-
Receiver operating characteristic
- AUC:
-
Area under the curve
References
Van Den Berg B, Walgaard C, Drenthen J et al (2014) Guillain-Barré syndrome: pathogenesis, diagnosis, treatment and prognosis [J]. Nat Rev Neurol 10(8):469–482
Liu S, Dong C, Ubogu EE (2018) Immunotherapy of Guillain-Barré syndrome [J]. Hum Vaccin Immunother 14(11):2568–2579
Shahrizaila N, Lehmann HC, Kuwabara S (2021) Guillain-Barré syndrome [J]. Lancet 397(10280):1214–1228
Brent GA (2012) Mechanisms of thyroid hormone action [J]. J Clin Invest 122(9):3035–3043
Zoeller RT, Rovet J (2004) Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings [J]. J Neuroendocrinol 16(10):809–818
Franco PG, Silvestroff L, Soto EF et al (2008) Thyroid hormones promote differentiation of oligodendrocyte progenitor cells and improve remyelination after cuprizone-induced demyelination [J]. Exp Neurol 212(2):458–467
Dell’Acqua ML, Lorenzini L, D’Intino G et al (2012) Functional and molecular evidence of myelin- and neuroprotection by thyroid hormone administration in experimental allergic encephalomyelitis [J]. Neuropathol Appl Neurobiol 38(5):454–470
Long Y, Zheng Y, Chen M, et al. (2014) Serum thyroid-stimulating hormone and anti-thyroglobulin antibody are independently associated with lesions in spinal cord in central nervous system demyelinating diseases [J]. PLoS One 9(8): e100672
Zhao W, Zeng H, Zhang X et al (2016) A high thyroid stimulating hormone level is associated with diabetic peripheral neuropathy in type 2 diabetes patients [J]. Diabetes Res Clin Pract 115:122–129
Umehara T, Matsuno H, Toyoda C et al (2015) Thyroid hormone level is associated with motor symptoms in de novo Parkinson’s disease [J]. J Neurol 262(7):1762–1768
Johansson P, Almqvist EG, Johansson JO et al (2013) Reduced cerebrospinal fluid level of thyroxine in patients with Alzheimer’s disease [J]. Psychoneuroendocrinology 38(7):1058–1066
Tozzoli R, Sorrentino MC, Bizzaro N (2013) Detecting multiple autoantibodies to diagnose autoimmune co-morbidity (multiple autoimmune syndromes and overlap syndromes): a challenge for the autoimmunologist [J]. Immunol Res 56(2–3):425–431
Kohli RS, Bleibel W, Bleibel H (2007) Concurrent immune thrombocytopenic purpura and Guillain-Barre syndrome in a patient with Hashimoto’s thyroiditis [J]. Am J Hematol 82(4):307–308
Toudou Daouda M, Obenda NS, Maazou L et al (2016) Guillain-Barre syndrome and Hashimoto’s thyroiditis [J]. QJM 109(8):547–548
Hughes RA, Newsom-Davis JM, Perkin GD et al (1978) Controlled trial prednisolone in acute polyneuropathy [J]. Lancet 2(8093):750–753
Kleyweg RP, Van Der Meché FG, Schmitz PI (1991) Interobserver agreement in the assessment of muscle strength and functional abilities in Guillain-Barré syndrome [J]. Muscle Nerve 14(11):1103–1109
Walgaard C, Lingsma HF, Ruts L et al (2010) Prediction of respiratory insufficiency in Guillain-Barré syndrome [J]. Ann Neurol 67(6):781–787
Naik GS, Meena AK, Reddy BAK et al (2017) Anti-ganglioside antibodies profile in Guillain-Barré syndrome: correlation with clinical features, electrophysiological pattern, and outcome [J]. Neurol India 65(5):1001–1005
Nobile-Orazio E (2001) Multifocal motor neuropathy [J]. J Neuroimmunol 115(1–2):4–18
McGonigal R, Rowan EG, Greenshields KN et al (2010) Anti-GD1a antibodies activate complement and calpain to injure distal motor nodes of Ranvier in mice [J]. Brain 133(Pt 7):1944–1960
Ahn SW, Kim SH, Park BS et al (2011) Concurrence of multifocal motor neuropathy and Hashimoto’s thyroiditis [J]. J Clin Neurol 7(3):168–172
Tu Y, Gong X, Zeng G, et al. (2020) Differences in thyroid function and autoantibodies in the development of Guillain-Barré syndrome vs. chronic inflammatory demyelinating polyradiculoneuropathy [J]. Front Neurol 11: 1018
Fishman PS, Shy ME, Hart DE et al (1991) Antibodies to the ganglioside GD1b in a patient with motor neuron disease and thyroid adenoma [J]. Arch Neurol 48(11):1188–1190
Beppu M, Sawai S, Misawa S et al (2015) Serum cytokine and chemokine profiles in patients with chronic inflammatory demyelinating polyneuropathy [J]. J Neuroimmunol 279:7–10
Karanikas G, Schuetz M, Wahl K et al (2005) Relation of anti-TPO autoantibody titre and T-lymphocyte cytokine production patterns in Hashimoto’s thyroiditis [J]. Clin Endocrinol (Oxf) 63(2):191–196
Kokkotou E, Marafelia P, Mantzos EI et al (2002) Serum monocyte chemoattractant protein-1 is increased in chronic autoimmune thyroiditis [J]. Metabolism 51(11):1489–1493
Comi C, Fleetwood T, Dianzani U (2012) The role of T cell apoptosis in nervous system autoimmunity [J]. Autoimmun Rev 12(2):150–156
Guzman-Rojas L, Sims-Mourtada JC, Rangel R et al (2002) Life and death within germinal centres: a double-edged sword [J]. Immunology 107(2):167–175
Li-Weber M, Krammer PH (2003) Function and regulation of the CD95 (APO-1/Fas) ligand in the immune system [J]. Semin Immunol 15(3):145–157
Bona G, Defranco S, Chiocchetti A et al (2003) Defective function of Fas in T cells from paediatric patients with autoimmune thyroid diseases [J]. Clin Exp Immunol 133(3):430–437
Gümüşyayla Ş, Vural G, Yurtoğullari Çevik Ş et al (2019) Dynamic thiol-disulphide homeostasis in patients with Guillain-Barre syndrome [J]. Neurol Res 41(5):413–418
Moog NK, Entringer S, Heim C et al (2017) Influence of maternal thyroid hormones during gestation on fetal brain development [J]. Neuroscience 342:68–100
Mohácsik P, Zeöld A, Bianco A C, et al. (2011) Thyroid hormone and the neuroglia: both source and target [J]. J Thyroid Res 2011: 215718
Crantz FR, Silva JE, Larsen PR (1982) An analysis of the sources and quantity of 3,5,3′-triiodothyronine specifically bound to nuclear receptors in rat cerebral cortex and cerebellum [J]. Endocrinology 110(2):367–375
Mancini A, Di Segni C, Raimondo S et al (2016) Thyroid hormones, oxidative stress, and inflammation [J]. Mediators Inflamm 2016:6757154
Zych-Twardowska E, Wajgt A (2001) Blood levels of selected hormones in patients with multiple sclerosis [J]. Med Sci Monit 7(5):1005–1012
Li Q, Qi X, Jia W (2016) 3,3′,5-Triiodothyroxine inhibits apoptosis and oxidative stress by the PKM2/PKM1 ratio during oxygen-glucose deprivation/reperfusion AC16 and HCM-a cells: T3 inhibits apoptosis and oxidative stress by PKM2/PKM1 ratio [J]. Biochem Biophys Res Commun 475(1):51–56
Huang Y, Ying Z, Chen Z et al (2017) Thyroid hormone level is associated with the frequency and severity of Guillain-Barré syndrome [J]. Int J Neurosci 127(10):893–899
Witsch J, Galldiks N, Bender A et al (2013) Long-term outcome in patients with Guillain-Barré syndrome requiring mechanical ventilation [J]. J Neurol 260(5):1367–1374
Green C, Baker T, Subramaniam A (2018) Predictors of respiratory failure in patients with Guillain-Barré syndrome: a systematic review and meta-analysis [J]. Med J Aust 208(4):181–188
Tan CY, Razali SNO, Goh KJ et al (2019) The utility of Guillain-Barré syndrome prognostic models in Malaysian patients [J]. J Peripher Nerv Syst 24(2):168–173
Podlaska M, Chełmińska M, Sworczak K (2003) Respiratory disorders in thyroid pathology] [J. Wiad Lek 56(9–10):468–474
Funding
This study was supported by grants from The First Hospital, Jilin University, Changchun, China, General Program of the National Natural Science Foundation (No. 81771299).
Author information
Authors and Affiliations
Contributions
Experimental design: Chunrong Li. Writing the manuscript and implementation of the experiment: Lingxin Kong. Data analysis: Xiujuan Wu, Yanwei Cheng, Kangding Liu, and Shan Liu.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Ethical approval
This study was approved by Ethics Committee of the Neuroscience Center, Department of Neurology, The First Hospital of Jilin University.
Informed consent
Informed consent was obtained from all patients and their legal representatives.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kong, L., Wu, X., Cheng, Y. et al. The prediction effects of thyroid function in the severity of Guillain-Barré syndrome. Neurol Sci 43, 5017–5028 (2022). https://doi.org/10.1007/s10072-022-06070-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10072-022-06070-3