Extended thymectomy for myasthenia gravis via subxiphoid versus intercostal approaches: A retrospective cohort study in a single center_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LU Gaojun , WANG Ruotian , LIU Baodong , SU Lei , QIAN Kun , ZHANG Peilong , ZHAO Teng ,  ZHANG Yi

Department of Thoracic Surgery, Xuanwu Hospital Capital Medical University, Beijing, 100032, P. R. China;

Corresponding author：

ZHANG Yi, Email: zhangyixwhosp@xwh.ccmu.edu.cn

Keywords：

Myasthenia gravis; extended thymectomy; surgical approaches; perioperative; prognosis

DOI：

10.7507/1007-4848.202310071

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Objective To analyze the clinical outcomes of extended thymectomy for myasthenia gravis (MG) patients under different surgical approaches, and to determine the factors affecting the prognosis of MG. Methods The MG patients who underwent extended thymectomy from January 2014 to March 2021 in our hospital were retrospectively collected. According to the surgical approach, they were divided into a subxiphoid group and an intercostal group, and the perioperative results and prognosis were compared between the two groups. A “good outcome” was defined as complete stable remission (CSR), pharmacological remission (PR) or minimal manifestations state (MMS); a “poor outcome” was defined as outcomes worse than MMS. Univariate and multivariate logistic regression analyses were performed to assess the factors associated with the good outcomes. Results A total of 187 MG patients were included in the study, including 82 males and 105 females, with a median age of 50 (36, 60) years. There were 134 patients in the intercostal group and 53 patients in the subxiphoid group. Compared with the intercostal group, although the operation time of the subxiphoid group was longer [200.0 (172.0, 232.0) min vs. 141.0 (118.0, 169.0) min, P<0.001], the intraoperative blood loss was less [10.0 (10.0, 20.0) mL vs. 20.0 (10.0, 50.0) mL, P<0.001], the postoperative hospital stay was shorter [3.0 (2.5, 4.0) d vs. 5.0 (3.0, 7.0) d, P<0.001], and the incidence of complications was lower [1 (1.9%) vs. 26 (19.4%), P=0.001]. A total of 159 (85.0%) patients were followed up for a median period of 46 (13, 99) months, with a good outcome rate of 90.6% and CSR rate of 33.3%. There were no statistical differences in PR, MMS or overall good outcome rates between the two groups (P>0.05). Multivariate logistic analysis showed that age≤50 years was an independent predictor for "good outcome" of MG patients. Conclusion Extended thymectomy via subxiphoid for MG is a safe, feasible and effective surgical approach.

Citation： LU Gaojun, WANG Ruotian, LIU Baodong, SU Lei, QIAN Kun, ZHANG Peilong, ZHAO Teng, ZHANG Yi. Extended thymectomy for myasthenia gravis via subxiphoid versus intercostal approaches: A retrospective cohort study in a single center. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(8): 1119-1126. doi: 10.7507/1007-4848.202310071 Copy

1.	Wolfe GI, Kaminski HJ, Aban IB, et al. Randomized trial of thymectomy in myasthenia gravis. N Engl J Med, 2016, 375(6): 511-522.
2.	Gilhus NE, Tzartos S, Evoli A, et al. Myasthenia gravis. Nat Rev Dis Primers, 2019, 5(1): 30.
3.	Gilhus NE. Myasthenia gravis. N Engl J Med, 2016, 375(26): 2570-2581.
4.	Burt BM, Yao X, Shrager J, et al. Determinants of complete resection of thymoma by minimally invasive and open thymectomy: Analysis of an international registry. J Thorac Oncol, 2017, 12(1): 129-136.
5.	Batirel HF. Minimally invasive techniques in thymic surgery: A worldwide perspective. J Vis Surg, 2018, 4: 7.
6.	Zieliński M, Kuzdzał J, Szlubowski A, et al. Transcervical-subxiphoid-videothoracoscopic "maximal" thymectomy: Operative technique and early results. Ann Thorac Surg, 2004, 78(2): 404-409.
7.	Cooper JD, Al-Jilaihawa AN, Pearson FG, et al. An improved technique to facilitate transcervical thymectomy for myasthenia gravis. Ann Thorac Surg, 1988, 45(3): 242-247.
8.	Marulli G, Rea F, Melfi F, et al. Robot-aided thoracoscopic thymectomy for early-stage thymoma: A multicenter European study. J Thorac Cardiovasc Surg, 2012, 144(5): 1125-1130.
9.	Marx A, Chan JK, Coindre JM, et al. The 2015 World Health Organization classification of tumors of the thymus: continuity and changes. J Thorac Oncol, 2015, 10(10): 1383-1395.
10.	Detterbeck FC, Nicholson AG, Kondo K, et al. The Masaoka-Koga stage classification for thymic malignancies: Clarification and definition of terms. J Thorac Oncol, 2011, 6(7 Suppl 3): S1710-S1716.
11.	Verschuuren JJ, Palace J, Murai H, et al. Advances and ongoing research in the treatment of autoimmune neuromuscular junction disorders. Lancet Neurol, 2022, 21(2): 189-202.
12.	Punga AR, Maddison P, Heckmann JM, et al. Epidemiology, diagnostics, and biomarkers of autoimmune neuromuscular junction disorders. Lancet Neurol, 2022, 21(2): 176-188.
13.	Narayanaswami P, Sanders DB, Wolfe G, et al. International consensus guidance for management of myasthenia gravis: 2020 update. Neurology, 2021, 96(3): 114-122.
14.	Wilshire CL, Blitz SL, Fuller CC, et al. Minimally invasive thymectomy for myasthenia gravis favours left-sided approach and low severity class. Eur J Cardiothorac Surg, 2021, 60(4): 898-905.
15.	Jiang L, Chen H, Hou Z, et al. Subxiphoid versus unilateral video-assisted thoracoscopic surgery thymectomy for thymomas: A propensity score matching analysis. Ann Thorac Surg, 2022, 113(5): 1656-1662.
16.	Cao P, Hu S, Qu W, et al. Subxiphoid-subcostal thoracoscopic thymectomy for seropositive myasthenia offers equivalent remission rates and potentially faster recovery. Interact Cardiovasc Thorac Surg, 2022, 34(4): 576-583.
17.	Suda T, Hachimaru A, Tochii D, et al. Video-assisted thoracoscopic thymectomy versus subxiphoid single-port thymectomy: Initial results. Eur J Cardiothorac Surg, 2016, 49 Suppl 1: i54-i58.
18.	Qiu Z, Chen L, Lin Q, et al. Perioperative outcomes and mid-term effects in performing video-assisted thoracoscopic extended thymectomy for myasthenia gravis: Subxiphoid versus right thoracic approaches. J Thorac Dis, 2020, 12(4): 1529-1539.
19.	Kaufman AJ, Palatt J, Sivak M, et al. Thymectomy for myasthenia gravis: Complete stable remission and associated prognostic factors in over 1000 cases. Semin Thorac Cardiovasc Surg, 2016, 28(2): 561-568.
20.	Tian W, Li X, Tong H, et al. Surgical effect and prognostic factors of myasthenia gravis with thymomas. Thorac Cancer, 2020, 11(5): 1288-1296.
21.	Liu Z, Yang J, Lin L, et al. Unilateral video-assisted thoracoscopic extended thymectomy offers long-term outcomes equivalent to that of the bilateral approach in the treatment of non-thymomatous myasthenia gravis. Interact Cardiovasc Thorac Surg, 2015, 21(5): 610-615.
22.	Xie X, Gan X, Chen B, et al. Left- and right-sided video-assisted thoracoscopic thymectomy exhibit similar effects on myasthenia gravis. J Thorac Dis, 2016, 8(1): 124-132.
23.	Álvarez-Velasco R, Gutiérrez-Gutiérrez G, Trujillo JC, et al. Clinical characteristics and outcomes of thymoma-associated myasthenia gravis. Eur J Neurol, 2021, 28(6): 2083-2091.
24.	Kim H, Lim YM, Lee EJ, et al. Factors predicting remission in thymectomized patients with acetylcholine receptor antibody-positive myasthenia gravis. Muscle Nerve, 2018, 58(6): 796-800.
25.	de Perrot M, Liu J, Bril V, et al. Prognostic significance of thymomas in patients with myasthenia gravis. Ann Thorac Surg, 2002, 74(5): 1658-1662.
26.	Liu CW, Luo M, Mei JD, et al. Perioperative and long-term outcome of thymectomy for myasthenia gravis: Comparison of surgical approaches and prognostic analysis. Chin Med J, 2013, 126(1): 34-40.

1. Wolfe GI, Kaminski HJ, Aban IB, et al. Randomized trial of thymectomy in myasthenia gravis. N Engl J Med, 2016, 375(6): 511-522.
2. Gilhus NE, Tzartos S, Evoli A, et al. Myasthenia gravis. Nat Rev Dis Primers, 2019, 5(1): 30.
3. Gilhus NE. Myasthenia gravis. N Engl J Med, 2016, 375(26): 2570-2581.
4. Burt BM, Yao X, Shrager J, et al. Determinants of complete resection of thymoma by minimally invasive and open thymectomy: Analysis of an international registry. J Thorac Oncol, 2017, 12(1): 129-136.
5. Batirel HF. Minimally invasive techniques in thymic surgery: A worldwide perspective. J Vis Surg, 2018, 4: 7.
6. Zieliński M, Kuzdzał J, Szlubowski A, et al. Transcervical-subxiphoid-videothoracoscopic "maximal" thymectomy: Operative technique and early results. Ann Thorac Surg, 2004, 78(2): 404-409.
7. Cooper JD, Al-Jilaihawa AN, Pearson FG, et al. An improved technique to facilitate transcervical thymectomy for myasthenia gravis. Ann Thorac Surg, 1988, 45(3): 242-247.
8. Marulli G, Rea F, Melfi F, et al. Robot-aided thoracoscopic thymectomy for early-stage thymoma: A multicenter European study. J Thorac Cardiovasc Surg, 2012, 144(5): 1125-1130.
9. Marx A, Chan JK, Coindre JM, et al. The 2015 World Health Organization classification of tumors of the thymus: continuity and changes. J Thorac Oncol, 2015, 10(10): 1383-1395.
10. Detterbeck FC, Nicholson AG, Kondo K, et al. The Masaoka-Koga stage classification for thymic malignancies: Clarification and definition of terms. J Thorac Oncol, 2011, 6(7 Suppl 3): S1710-S1716.
11. Verschuuren JJ, Palace J, Murai H, et al. Advances and ongoing research in the treatment of autoimmune neuromuscular junction disorders. Lancet Neurol, 2022, 21(2): 189-202.
12. Punga AR, Maddison P, Heckmann JM, et al. Epidemiology, diagnostics, and biomarkers of autoimmune neuromuscular junction disorders. Lancet Neurol, 2022, 21(2): 176-188.
13. Narayanaswami P, Sanders DB, Wolfe G, et al. International consensus guidance for management of myasthenia gravis: 2020 update. Neurology, 2021, 96(3): 114-122.
14. Wilshire CL, Blitz SL, Fuller CC, et al. Minimally invasive thymectomy for myasthenia gravis favours left-sided approach and low severity class. Eur J Cardiothorac Surg, 2021, 60(4): 898-905.
15. Jiang L, Chen H, Hou Z, et al. Subxiphoid versus unilateral video-assisted thoracoscopic surgery thymectomy for thymomas: A propensity score matching analysis. Ann Thorac Surg, 2022, 113(5): 1656-1662.
16. Cao P, Hu S, Qu W, et al. Subxiphoid-subcostal thoracoscopic thymectomy for seropositive myasthenia offers equivalent remission rates and potentially faster recovery. Interact Cardiovasc Thorac Surg, 2022, 34(4): 576-583.
17. Suda T, Hachimaru A, Tochii D, et al. Video-assisted thoracoscopic thymectomy versus subxiphoid single-port thymectomy: Initial results. Eur J Cardiothorac Surg, 2016, 49 Suppl 1: i54-i58.
18. Qiu Z, Chen L, Lin Q, et al. Perioperative outcomes and mid-term effects in performing video-assisted thoracoscopic extended thymectomy for myasthenia gravis: Subxiphoid versus right thoracic approaches. J Thorac Dis, 2020, 12(4): 1529-1539.
19. Kaufman AJ, Palatt J, Sivak M, et al. Thymectomy for myasthenia gravis: Complete stable remission and associated prognostic factors in over 1000 cases. Semin Thorac Cardiovasc Surg, 2016, 28(2): 561-568.
20. Tian W, Li X, Tong H, et al. Surgical effect and prognostic factors of myasthenia gravis with thymomas. Thorac Cancer, 2020, 11(5): 1288-1296.
21. Liu Z, Yang J, Lin L, et al. Unilateral video-assisted thoracoscopic extended thymectomy offers long-term outcomes equivalent to that of the bilateral approach in the treatment of non-thymomatous myasthenia gravis. Interact Cardiovasc Thorac Surg, 2015, 21(5): 610-615.
22. Xie X, Gan X, Chen B, et al. Left- and right-sided video-assisted thoracoscopic thymectomy exhibit similar effects on myasthenia gravis. J Thorac Dis, 2016, 8(1): 124-132.
23. Álvarez-Velasco R, Gutiérrez-Gutiérrez G, Trujillo JC, et al. Clinical characteristics and outcomes of thymoma-associated myasthenia gravis. Eur J Neurol, 2021, 28(6): 2083-2091.
24. Kim H, Lim YM, Lee EJ, et al. Factors predicting remission in thymectomized patients with acetylcholine receptor antibody-positive myasthenia gravis. Muscle Nerve, 2018, 58(6): 796-800.
25. de Perrot M, Liu J, Bril V, et al. Prognostic significance of thymomas in patients with myasthenia gravis. Ann Thorac Surg, 2002, 74(5): 1658-1662.
26. Liu CW, Luo M, Mei JD, et al. Perioperative and long-term outcome of thymectomy for myasthenia gravis: Comparison of surgical approaches and prognostic analysis. Chin Med J, 2013, 126(1): 34-40.

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Extended thymectomy for myasthenia gravis via subxiphoid versus intercostal approaches: A retrospective cohort study in a single center

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