Unexpected Transient Glioblastoma Regression in a Patient Previously Treated with Bacillus Calmette–Guérin Therapy: A Case Report and Immunomodulatory Effects Hypothesis
Abstract
1. Introduction
2. Case Presentation
2.1. Clinical Examination and Findings
2.2. Imaging and Initial Diagnosis
2.3. Further Diagnostic Tests
2.4. Initial Surgical Intervention
2.5. Histological Examination
2.6. Treatment and Follow-Up
2.7. Disease Progression
2.8. End-of-Life Care
3. Discussion
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sandes, E.; Lodillinsky, C.; Cwirenbaum, R.; Argüelles, C.; Casabé, A.; Eiján, A.M. Cathepsin B is involved in the apoptosis intrinsic pathway induced by Bacillus Calmette-Guérin in transitional cancer cell lines. Int. J. Mol. Med. 2007, 20, 823–828. [Google Scholar] [CrossRef]
- Yu, D.S.; Wu, C.L.; Ping, S.Y.; Keng, C.; Shen, K.H. Bacille Calmette-Guerin can induce cellular apoptosis of urothelial cancer directly through toll-like receptor 7 activation. Kaohsiung J. Med. Sci. 2015, 31, 391–397. [Google Scholar] [CrossRef] [PubMed]
- Choi, S.Y.; Kim, S.J.; Chi, B.H.; Kwon, J.K.; Chang, I.H. Modulating the internalization of bacille Calmette-Guérin by cathelicidin in bladder cancer cells. Urology 2015, 85, 964.e7–964.e12. [Google Scholar] [CrossRef] [PubMed]
- Geckin, B.; Konstantin Föhse, F.; Domínguez-Andrés, J.; Netea, M.G. Trained immunity: Implications for vaccination. Curr. Opin. Immunol. 2022, 77, 102190. [Google Scholar] [CrossRef] [PubMed]
- Holla, S.; Ghorpade, D.S.; Singh, V.; Bansal, K.; Balaji, K.N. Mycobacterium bovis BCG promotes tumor cell survival from tumor necrosis factor-α-induced apoptosis. Mol. Cancer 2014, 13, 210. [Google Scholar] [CrossRef] [PubMed]
- Ryk, C.; Koskela, L.R.; Thiel, T.; Wiklund, N.P.; Steineck, G.; Schumacher, M.C.; de Verdier, P.J. Outcome after BCG treatment for urinary bladder cancer may be influenced by polymorphisms in the NOS2 and NOS3 genes. Redox Biol. 2015, 6, 272–277. [Google Scholar] [CrossRef] [PubMed]
- Biau, J.; Chautard, E.; De Schlichting, E.; Dupic, G.; Pereira, B.; Fogli, A.; Müller-Barthélémy, M.; Dalloz, P.; Khalil, T.; Dillies, A.F.; et al. Radiotherapy plus temozolomide in elderly patients with GBM: A “real-life” report. Radiat. Oncol. 2017, 12, 197. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, K.; Udono-Fujimori, R.; Totsune, K.; Murakami, O.; Shibahara, S. Suppression of cytokine-induced expression of adrenomedullin and endothelin-1 by dexamethasone in T98G human GBM cells. Peptides 2003, 24, 1053–1062. [Google Scholar] [CrossRef]
- Li, X.N.; Shu, Q.; Su, J.M.; Perlaky, L.; Blaney, S.M.; Lau, C.C. Valproic acid induces growth arrest, apoptosis, and senescence in medulloblastomas by increasing histone hyperacetylation and regulating expression of p21Cip1, CDK4, and CMYC. Mol. Cancer Ther. 2005, 4, 1912–1922. [Google Scholar] [CrossRef]
- Peddi, P.; Ajit, N.E.; Burton, G.V.; El-Osta, H. Regression of a glioblastoma multiforme: Spontaneous versus a potential antineoplastic effect of dexamethasone and levetiracetam. BMJ Case Rep. 2016, 2016, bcr2016217393. [Google Scholar] [CrossRef]
- Sindoni, A.; Severo, C.; Vadala’, R.E.; Ferini, G.; Mazzei, M.M.; Vaccaro, M.; IatÌ, G.; Pontoriero, A.; Pergolizzi, S. Levetiracetam-induced radiation recall dermatitis in a patient undergoing stereotactic radiotherapy. J. Dermatol. 2016, 43, 1440–1441. [Google Scholar] [CrossRef]
- Hwang, K.; Kim, J.; Kang, S.G.; Jung, T.Y.; Kim, J.H.; Kim, S.H.; Kang, S.H.; Hong, Y.K.; Kim, T.M.; Kim, Y.J.; et al. Levetiracetam as a sensitizer of concurrent chemoradiotherapy in newly diagnosed glioblastoma: An open-label phase 2 study. Cancer Med. 2022, 11, 371–379. [Google Scholar] [CrossRef]
- Pallud, J.; Huberfeld, G.; Dezamis, E.; Peeters, S.; Moiraghi, A.; Gavaret, M.; Guinard, E.; Dhermain, F.; Varlet, P.; Oppenheim, C.; et al. Effect of Levetiracetam Use Duration on Overall Survival of Isocitrate Dehydrogenase Wild-Type Glioblastoma in Adults: An Observational Study. Neurology 2022, 98, e125–e140. [Google Scholar] [CrossRef]
- Roh, T.H.; Moon, J.H.; Park, H.H.; Kim, E.H.; Hong, C.K.; Kim, S.H.; Kang, S.G.; Chang, J.H. Association between survival and levetiracetam use in glioblastoma patients treated with temozolomide chemoradiotherapy. Sci. Rep. 2020, 10, 10783. [Google Scholar] [CrossRef]
- Kim, Y.H.; Kim, T.; Joo, J.D.; Han, J.H.; Kim, Y.J.; Kim, I.A.; Yun, C.H.; Kim, C.Y. Survival benefit of levetiracetam in patients treated with concomitant chemoradiotherapy and adjuvant chemotherapy with temozolomide for glioblastoma multiforme. Cancer 2015, 121, 2926–2932. [Google Scholar] [CrossRef]
- Kumar, A.A.; Abraham Koshy, A. Regression of Recurrent High-Grade Glioma with Temozolomide, Dexamethasone, and Levetiracetam: Case Report and Review of the Literature. World Neurosurg. 2017, 108, 990.e11–990.e16. [Google Scholar] [CrossRef]
- Albright, L.; Seab, J.A.; Ommaya, A.K. Intracerebral delayed hypersensitivity reactions in GBM multiforme patients. Cancer 1977, 39, 1331–1336. [Google Scholar] [CrossRef]
- Knerich, R.; Robustelli della Cuna, G.; Butti, G.; Pavesi, L.; Adinolfi, D.; Preti, P.; Locatelli, D. Chemotherapy plus immunotherapy for patients with primary and metastatic brain tumors. J. Neurosurg. Sci. 1985, 29, 19–24. [Google Scholar]
- Albright, L.; Madigan, J.C.; Gaston, M.R.; Houchens, D.P. Therapy in an intracerebral murine glioma model, using Bacillus Calmette-Guérin, neuraminidase-treated tumor cells, and 1-(2-chloroethyl)-3-cyclohexyl-1-nitrosourea. Cancer Res. 1975, 35, 658–665. [Google Scholar]
- Wikstrand, C.J.; Bigner, D.D. Hyperimmunization of non-human primates with BCG-CW and cultured human glioma-derived cells. Production of reactive antisera and absence of EAE induction. J. Neuroimmunol. 1981, 1, 249–260. [Google Scholar] [CrossRef]
- Holladay, F.P.; Heitz-Turner, T.; Bayer, W.L.; Wood, G.W. Autologous tumor cell vaccination combined with adoptive cellular immunotherapy in patients with grade III/IV astrocytoma. J. Neurooncol. 1996, 27, 179–189. [Google Scholar] [CrossRef] [PubMed]
- van Puffelen, J.H.; Keating, S.T.; Oosterwijk, E.; van der Heijden, A.G.; Netea, M.G.; Joosten, L.A.B.; Vermeulen, S.H. Trained immunity as a molecular mechanism for BCG immunotherapy in bladder cancer. Nat. Rev. Urol. 2020, 17, 513–525. [Google Scholar] [CrossRef] [PubMed]
- Parlato, C.; Barbarisi, M.; Moraci, M.; Moraci, A. Surgery, radiotherapy and temozolomide in treating high-grade gliomas. Front. Biosci. 2006, 11, 1280–1283. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Laigle-Donadey, F.; Figarella-Branger, D.; Chinot, O.; Taillandier, L.; Cartalat-Carel, S.; Honnorat, J.; Kaloshi, G.; Delattre, J.Y.; Sanson, M. Up-front temozolomide in elderly patients with glioblastoma. J. Neurooncol. 2010, 99, 89–94. [Google Scholar] [CrossRef] [PubMed]
- Yamasaki, F.; Takayasu, T.; Nosaka, R.; Haratake, D.; Arihiro, K.; Ueno, H.; Shimomura, R.; Akiyama, Y.; Sugiyama, K.; Matsumoto, M.; et al. Transient spontaneous regression of brainstem glioblastoma. J. Neurosurg. Sci. 2018, 62, 610–612. [Google Scholar] [CrossRef] [PubMed]
- Gandhoke, C.S.; Ansari, M.T.; Syal, S.K.; Singh, D.; Saran, R.K. Spontaneous Regression of a Suspected Temporal lobe Glioblastoma Multiforme and its Re-appearance at a Different Site. JCR 2017, 7, 214–218. [Google Scholar] [CrossRef][Green Version]
- Zhang, Y.; Zhang, Z. The history and advances in cancer immunotherapy: Understanding the characteristics of tumor-infiltrating immune cells and their therapeutic implications. Cell Mol. Immunol. 2020, 17, 807–821. [Google Scholar] [CrossRef]
- Žarković, N.; Jaganjac, M.; Žarković, K.; Gęgotek, A.; Skrzydlewska, E. Spontaneous Regression of Cancer: Revealing Granulocytes and Oxidative Stress as the Crucial Double-edge Sword. Front. Biosci. (Landmark Ed.) 2022, 27, 119. [Google Scholar] [CrossRef]
- Pokhrel, B.; Chidharla, A.; Neupane, P. Spontaneous Regression of the Pulmonary Metastases in Adenoid Cystic Carcinoma of the Parotid Gland: A Case Report. Cureus 2022, 14, e30783. [Google Scholar] [CrossRef]
- Roseman, J.M. Regression of locally recurrent squamous cell carcinoma of the skin following excision of a metastasis: With review of the literature. J. Surg. Oncol. 1988, 39, 213–214. [Google Scholar] [CrossRef]
- Arrieta, V.A.; Dmello, C.; McGrail, D.J.; Brat, D.J.; Lee-Chang, C.; Heimberger, A.B.; Chand, D.; Stupp, R.; Sonabend, A.M. Immune checkpoint blockade in glioblastoma: From tumor heterogeneity to personalized treatment. J. Clin. Investig. 2023, 133, e163447. [Google Scholar] [CrossRef]
- Ghouzlani, A.; Kandoussi, S.; Tall, M.; Reddy, K.P.; Rafii, S.; Badou, A. Immune Checkpoint Inhibitors in Human Glioma Microenvironment. Front. Immunol. 2021, 12, 679425. [Google Scholar] [CrossRef]
- Qi, Y.; Liu, B.; Sun, Q.; Xiong, X.; Chen, Q. Immune Checkpoint Targeted Therapy in Glioma: Status and Hopes. Front. Immunol. 2020, 11, 578877. [Google Scholar] [CrossRef]
- Croese, T.; Castellani, G.; Schwartz, M. Immune cell compartmentalization for brain surveillance and protection. Nat. Immunol. 2021, 22, 1083–1092. [Google Scholar] [CrossRef]
- Pardoll, D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 2012, 12, 252–264. [Google Scholar] [CrossRef]
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Scalia, G.; Ferini, G.; Marrone, S.; Salvati, M.; Yamamoto, V.; Kateb, B.; Schulte, R.; Forte, S.; Umana, G.E. Unexpected Transient Glioblastoma Regression in a Patient Previously Treated with Bacillus Calmette–Guérin Therapy: A Case Report and Immunomodulatory Effects Hypothesis. J. Pers. Med. 2023, 13, 1661. https://doi.org/10.3390/jpm13121661
Scalia G, Ferini G, Marrone S, Salvati M, Yamamoto V, Kateb B, Schulte R, Forte S, Umana GE. Unexpected Transient Glioblastoma Regression in a Patient Previously Treated with Bacillus Calmette–Guérin Therapy: A Case Report and Immunomodulatory Effects Hypothesis. Journal of Personalized Medicine. 2023; 13(12):1661. https://doi.org/10.3390/jpm13121661
Chicago/Turabian StyleScalia, Gianluca, Gianluca Ferini, Salvatore Marrone, Maurizio Salvati, Vicky Yamamoto, Babak Kateb, Reinhard Schulte, Stefano Forte, and Giuseppe Emmanuele Umana. 2023. "Unexpected Transient Glioblastoma Regression in a Patient Previously Treated with Bacillus Calmette–Guérin Therapy: A Case Report and Immunomodulatory Effects Hypothesis" Journal of Personalized Medicine 13, no. 12: 1661. https://doi.org/10.3390/jpm13121661
APA StyleScalia, G., Ferini, G., Marrone, S., Salvati, M., Yamamoto, V., Kateb, B., Schulte, R., Forte, S., & Umana, G. E. (2023). Unexpected Transient Glioblastoma Regression in a Patient Previously Treated with Bacillus Calmette–Guérin Therapy: A Case Report and Immunomodulatory Effects Hypothesis. Journal of Personalized Medicine, 13(12), 1661. https://doi.org/10.3390/jpm13121661