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Thymectomy is a beneficial therapy for patients with non-thymomatous ocular myasthenia gravis: a systematic review and meta-analysis

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Abstract

Ocular myasthenia gravis, an autoimmune disease, is characterized by extraocular muscle weakness. Myasthenia gravis is closely associated with the functional status of the thymus gland. The efficacy of thymectomy for non-thymomatous ocular myasthenia gravis remains controversial. Here, we present the first systematic review and meta-analysis of studies assessing the outcome of thymectomy in patients with non-thymomatous ocular myasthenia gravis and found that the pooled rate of complete stable remission was 0.5074 with considerable heterogeneity. Furthermore, subgroup analysis showed that the efficacy of thymectomy differed according to geographical location. Furthermore, thymectomy outcomes are better in children than they are in adults. Thymectomy clearly represents an effective treatment for patients with non-thymomatous ocular myasthenia gravis. However, more multicenter, randomized, controlled clinical trials are now required to confirm these conclusions.

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References

  1. Gilhus NE, Skeie GO, Romi F et al (2016) Myasthenia gravis—autoantibody characteristics and their implications for therapy. Nat Rev Neurol 12:259–268. doi:10.1038/nrneurol.2016.44

    Article  CAS  PubMed  Google Scholar 

  2. Gilhus NE, Verschuuren JJ (2015) Myasthenia gravis: subgroup classification and therapeutic strategies. Lancet Neurol 14:1023–1036

    Article  CAS  PubMed  Google Scholar 

  3. Bever CTJ, Aquino AV, Penn AS et al (1983) Prognosis of ocular myasthenia. Ann Neurol 14:516–519

    Article  PubMed  Google Scholar 

  4. Liu WB (2011) Ocular myasthenia gravis research progress and clinical problems. Chin J Neuroimmunol Neurol 5:314–316

    Google Scholar 

  5. Cea G, Benatar M, Verdugo RJ, Salinas RA (2013) Thymectomy for non-thymomatous myasthenia gravis. Cochrane Database Syst Rev CD008111. doi:10.1002/14651858.CD008111.pub2

  6. Yang DS, Nakahara K, Ohno K et al (1989) The result of extended thymectomy in patients with myasthenia gravis of pure ocular type. Nihon Kyobu Geka Gakkai Zasshi 37:313–317

    CAS  PubMed  Google Scholar 

  7. Schumm F, Wietholter H, Fateh-Moghadam A, Dichgans J (1985) Thymectomy in myasthenia with pure ocular symptoms. J Neurol Neurosurg Psychiatry 48:332–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kodama H, Yoshida I, Iijima T et al (1993) Effect of extended thymectomy in myasthenia gravis of pure ocular type. Kyobu Geka 46:1017–1020

    CAS  PubMed  Google Scholar 

  9. Mineo TC, Ambrogi V (2013) Outcomes after thymectomy in class I myasthenia gravis. J Thorac Cardiovasc Surg 145:1319–1324

    Article  PubMed  Google Scholar 

  10. Kawaguchi N, Kuwabara S, Nemoto Y et al (2004) Treatment and outcome of myasthenia gravis: retrospective multi-center analysis of 470 Japanese patients, 1999-2000. J Neurol Sci 224:43–47

    Article  PubMed  Google Scholar 

  11. Papatestas AE, Genkins G, Kornfeld P et al (1987) Effects of thymectomy in myasthenia gravis. Ann Surg 206:79–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8:336–341. doi:10.1016/j.ijsu.2010.02.007

    Article  PubMed  Google Scholar 

  13. Jaretzki AR, Barohn RJ, Ernstoff RM et al (2000) Myasthenia gravis: recommendations for clinical research standards. Task force of the medical scientific advisory Board of the Myasthenia Gravis Foundation of America. Neurology 55:16–23

    Article  PubMed  Google Scholar 

  14. Osserman KE, Genkins G (1971) Studies in myasthenia gravis: review of a twenty-year experience in over 1200 patients. Mt Sinai J Med 38:497–537

    CAS  PubMed  Google Scholar 

  15. Stroup DF, Berlin JA, Morton SC et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283:2008–2012

    Article  CAS  PubMed  Google Scholar 

  16. Vandenbroucke JP, von Elm E, Altman DG et al (2014) Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. Int J Surg 12:1500–1524. doi:10.1016/j.ijsu.2014.07.014

    Article  PubMed  Google Scholar 

  17. O’Connor AM, Sargeant JM, Dohoo IR et al (2016) Explanation and elaboration document for the STROBE-vet statement: strengthening the reporting of observational studies in epidemiology—veterinary extension. Zoonoses Public Health 63:662–698. doi:10.1111/zph.12315

    Article  PubMed  Google Scholar 

  18. Schwarzer G 2006 Meta-analysis of single proportions. http://artax.karlin.mff.cuni.cz/r-help/library/meta/html/metaprop.html. Accessed 26 May 2017

  19. Luo ML, Tan HZ, Zhou Q et al (2013) Reallizing the meta-analysis of single rate in R software. J Evid Based Med 3:181–184,188

    Google Scholar 

  20. Masaoka A, Yamakawa Y, Niwa H et al (1996) Extended thymectomy for myasthenia gravis patients: a 20-year review. Ann Thorac Surg 62:853–859

    Article  CAS  PubMed  Google Scholar 

  21. Nakamura H, Taniguchi Y, Suzuki Y et al (1996) Delayed remission after thymectomy for myasthenia gravis of the purely ocular type. J Thorac Cardiovasc Surg 112:371–375

    Article  CAS  PubMed  Google Scholar 

  22. Ti T, Ji ZD, Yan SP et al (1996) Surgery of ocular myasthenia gravis in children. Chin J Ped Surg 17:360

    Google Scholar 

  23. Chen JM, Jiang YG, Shizhi F et al (2000) Surgical treatment of myasthenia gravis in children. Chin J Clin Thorac Cardiovasc Surg 1:10–12

    Google Scholar 

  24. Roberts PF, Venuta F, Rendina E et al (2001) Thymectomy in the treatment of ocular myasthenia gravis. J Thorac Cardiovasc Surg 122:562–568

    Article  CAS  PubMed  Google Scholar 

  25. Singh RS, Behera SK, Saji R, Dhaliwal RS (2003) Thymectomy for myasthenia gravis: 12-year experience. Asian Cardiovasc Thorac Ann 11:299–303

    Article  PubMed  Google Scholar 

  26. Tansel T, Onursal E, Barlas S et al (2003) Results of surgical treatment for nonthymomatous myasthenia gravis. Surg Today 33:666–670

    Article  PubMed  Google Scholar 

  27. Zielinski M, Kuzdzal J, Szlubowski A, Soja J (2004) Comparison of late results of basic transsternal and extended transsternal thymectomies in the treatment of myasthenia gravis. Ann Thorac Surg 78:253–258

    Article  PubMed  Google Scholar 

  28. Zhang CB, Zheng J, Wang Q et al (2004) Treatment of 20 ocular myasthenia gravis cases. J Zhengzhou Univ 39:914–915

    Google Scholar 

  29. Tan QY, Wang RW, Jiang YG et al (2004) Long-term outcome and relevant factors of thymectomy for myasthenia gravis in children. Chin J Surg 2:177–178

    Google Scholar 

  30. Lu JJ, Zhong FT, Li XR et al (2004) Surgical treatment of myasthenia gravis in children. Guangdong Med J 4:430–431

    Google Scholar 

  31. Rea F, Marulli G, Bortolotti L et al (2006) Experience with the “da Vinci” robotic system for thymectomy in patients with myasthenia gravis: report of 33 cases. Ann Thorac Surg 81:455–459

    Article  PubMed  Google Scholar 

  32. Wang H, Zhou L, Gao Y et al (2007) Thymectomy of myasthenia gravis in children. J Brain Nerv Dis 2:134–135

    Google Scholar 

  33. Luo LQ, Zhang JZ, Cui HN et al (2008) Clinical analysis of thymectomy for juvenile with myasthenia gravis. China J Mod Med 15:2202–2204

    Google Scholar 

  34. Prokakis C, Koletsis E, Salakou S et al (2009) Modified maximal thymectomy for myasthenia gravis: effect of maximal resection on late neurologic outcome and predictors of disease remission. Ann Thorac Surg 88:1638–1645

    Article  PubMed  Google Scholar 

  35. Pompeo E, Tacconi F, Massa R et al (2009) Long-term outcome of thoracoscopic extended thymectomy for nonthymomatous myasthenia gravis. Eur J Cardiothorac Surg 36:164–169

    Article  PubMed  Google Scholar 

  36. Deng Y, Zhang X (2009) Prognosis of thymectomy in treatment of ocular myasthenia gravis and relevant influencing factors. Natl Med J China 89:1922–1925

    Google Scholar 

  37. Lin MW, Chang YL, Huang PM, Lee YC (2010) Thymectomy for non-thymomatous myasthenia gravis: a comparison of surgical methods and analysis of prognostic factors. Eur J Cardiothorac Surg 37:7–12

    Article  PubMed  Google Scholar 

  38. Xie SP, Jie H (2010) The analysis of thymectomy for pure ocular myasthenia gravis in children. J Clin Surg 18:40–41

    Google Scholar 

  39. Liu Z, Feng H, Yeung SC et al (2011) Extended transsternal thymectomy for the treatment of ocular myasthenia gravis. Ann Thorac Surg 92:1993–1999

    Article  PubMed  Google Scholar 

  40. Cheng C, Liu Z, Xu F et al (2013) Clinical outcome of juvenile myasthenia gravis after extended transsternal thymectomy in a Chinese cohort. Ann Thorac Surg 95:1035–1041

    Article  PubMed  Google Scholar 

  41. Huang CS, Li WY, Lee PC et al (2014) Analysis of outcomes following surgical treatment of thymolipomatous myasthenia gravis: comparison with thymomatous and non-thymomatous myasthenia gravis. Interact Cardiovasc Thorac Surg 18:475–481

    Article  PubMed  Google Scholar 

  42. Yan L, Liu WB et al (2012) Response to thymectomy and analysis of influencing factors in the treatment of children with myasthenia gravis. Zhonghua Yi Xue Za Zhi 92:1170–1173

    Google Scholar 

  43. Mineo TC, Ambrogi V, Schillaci O (2014) May positron emission tomography reveal ectopic or active thymus in preoperative evaluation of non-thymomatous myasthenia gravis? J Cardiothorac Surg 9:146

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ware TL, Ryan MM, Kornberg AJ (2012) Autoimmune myasthenia gravis, immunotherapy and thymectomy in children. Neuromuscul Disord 22:118–121

    Article  PubMed  Google Scholar 

  45. Wolfe GI, Kaminski HJ, Aban IB et al (2016) Randomized trial of thymectomy in myasthenia gravis. N Engl J Med 375:511–522. doi:10.1056/NEJMoa1602489

    Article  PubMed  PubMed Central  Google Scholar 

  46. Kaufman AJ, Palatt J, Sivak M et al (2016) Thymectomy for myasthenia gravis: complete stable remission and associated prognostic factors in over 1000 cases. Semin Thorac Cardiovasc Surg 28:561–568. doi:10.1053/j.semtcvs.2016.04.002

    Article  PubMed  Google Scholar 

  47. Kang SY, Oh JH, Song SK et al (2015) Both binding and blocking antibodies correlate with disease severity in myasthenia gravis. Neurol Sci 36:1167–1171. doi:10.1007/s10072-015-2236-8

    Article  PubMed  Google Scholar 

  48. Feng H-Y, Wang H-Y, Liu W-B et al (2013) The high frequency and clinical feature of seronegative myasthenia gravis in southern China. Neurol Sci 34:919–924. doi:10.1007/s10072-012-1159-x

    Article  CAS  PubMed  Google Scholar 

  49. Huang X, Liu WB, Men LN et al (2013) Clinical features of myasthenia gravis in southern China: a retrospective review of 2,154 cases over 22 years. Neurol Sci 34:911–917. doi:10.1007/s10072-012-1157-z

    Article  CAS  PubMed  Google Scholar 

  50. Wang W, Chen YP, Wang ZK et al (2013) A cohort study on myasthenia gravis patients in China. Neurol Sci 34:1759–1764. doi:10.1007/s10072-013-1329-5

    Article  CAS  PubMed  Google Scholar 

  51. Benatar M, Sanders DB, Wolfe GI et al (2012) Design of the efficacy of prednisone in the treatment of ocular myasthenia (EPITOME) trial. Ann N Y Acad Sci 1275:17–22. doi:10.1111/j.1749-6632.2012.06780.x

    Article  CAS  PubMed  Google Scholar 

  52. Friedant AJ, Handorf EA, Su S, Scott WJ (2016) Minimally invasive versus open thymectomy for thymic malignancies: systematic review and meta-analysis. J Thorac Oncol 11:30–38. doi:10.1016/j.jtho.2015.08.004

    Article  PubMed  Google Scholar 

  53. Yang Y, Dong J, Huang Y (2016) Thoracoscopic thymectomy versus open thymectomy for the treatment of thymoma: a meta-analysis. Eur J Surg Oncol 42:1720–1728. doi:10.1016/j.ejso.2016.03.029

    Article  CAS  PubMed  Google Scholar 

  54. Gung Y, Zhang H, Li S, Wang Y (2016) Sternotomy versus video-assisted thoracoscopic surgery for thymectomy of myasthenia gravis patients: a meta-analysis. Asian J Endosc Surg 9:285–294. doi:10.1111/ases.12300

    Article  PubMed  Google Scholar 

  55. Okusanya OT, Hess N, Christie N et al (2016) Improved outcomes with surgery vs. medical therapy in non-thymomatous myasthenia gravis: a perspective on the results of a randomized trial. Ann Transl Med 4:526. doi:10.21037/atm.2016.12.54

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the Project of Guangzhou Science Technology and Innovation Commission (grant number 201605122112149), the Undergraduate teaching reform project of Sun-Yat Sen university (grant number 8000031911105), and Guangdong graduate education innovation program (grant number 2015QTLXXM05).

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  1. Kai Zhu and Jiaoxing Li contributed equally to this work.

Authors and Affiliations

  1. Department of Neurology, the First Affiliated Hospital, Sun Yat-sen University, 58 Zhongshan 2nd Road, Guangzhou, 510080, China

    Kai Zhu, Jiaoxing Li, Xin Huang, Wei Xu, Weibin Liu, Jiaxin Chen, Pei Chen & Huiyu Feng

  2. Guangdong Provincial Key Laboratory for Diagnosis and Treatment of Major Neurological Disease, Guangdong, China

    Kai Zhu, Jiaoxing Li, Xin Huang, Wei Xu, Weibin Liu, Jiaxin Chen, Pei Chen & Huiyu Feng

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  1. Kai Zhu
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Correspondence to Huiyu Feng.

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Zhu, K., Li, J., Huang, X. et al. Thymectomy is a beneficial therapy for patients with non-thymomatous ocular myasthenia gravis: a systematic review and meta-analysis. Neurol Sci 38, 1753–1760 (2017). https://doi.org/10.1007/s10072-017-3058-7

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