Letter to the Editor. Feasibility and safety of supratotal resection for low-grade gliomas

Lesheng Wang MM and Jincao Chen MD, PhD
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  • Zhongnan Hospital of Wuhan University, Wuhan, China
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TO THE EDITOR: We read with great interest the article by Rossi et al.1 on the feasibility and safety of supratotal resection (STR) for low-grade gliomas (LGGs) (Rossi M, Ambrogi F, Gay L, et al. Is supratotal resection achievable in low-grade gliomas? Feasibility, putative factors, safety, and functional outcome. J Neurosurg. 2020;132[6]:1692–1705). At the outset, we congratulate the authors for reporting a large series of LGGs. They also deserve to be praised for their conclusion that STR is feasible and safe in routine surgery for LGGs. According to Rossi and colleagues, their study is the first to describe the feasibility and safety of STR for LGGs in routine clinical practice. In the meantime, we would like to express our respect for their achievements and share some comments with them.

First, the authors defined STR as the complete removal of any signal abnormalities, with the volume of the postoperative cavity being larger than the preoperative tumor volume. However, there are different definitions of STR in anatomy and radiology. Moreover, conventional MRI underestimates the spatial extent of LGG since tumor cells have been found up to 20 mm around MRI abnormalities. Because of the frequent location of LGGs within “eloquent” brain areas, it is often difficult to achieve STR.2 We believe that this definition has some defects because the microstructure of the tumor cannot be fully recognized under the microscope and because the bleeding site can also show abnormal signals on MRI, which interferes with clinicians’ judgment of the outcome of STR. Therefore, we think that postoperative pathological examination is very necessary. Whether LGGs are supratotally resected depends on the pathological results.

Second, in their paper, the authors mentioned that the possible influencing factors for STR include 1) factors related to the patient; 2) tumor-related factors that could be deduced by evaluating preoperative conventional MRI; 3) intraoperative factors such as the location of subcortical functional borders or previous biopsy or recurrence; and 4) integrated molecular/histological diagnosis, histological grade, and IDH1 mutation. Yet, we believe that another more significant factor may be the important blood vessels around or inside the tumor. If blood vessels in the tumor site are important arteries or large veins, intracranial hemorrhage can occur in patients during and after the operation, thus affecting the surgical outcome.

Third, total and supratotal resections were significantly higher in tumors with a frontal or temporal location, and subtotal/partial resections were significantly higher in tumors with an insular location (respectively, p < 0.001). Then the authors concluded that the incidence of permanent neurological deficits was low in all resection groups but was significantly higher in patients in the subtotal/partial resection group in comparison to the total or supratotal groups. However, because of the significant difference in tumor location among the three groups, there are contradictory statistics with regard to the conclusion that the incidence of a permanent neurological deficit in the subtotal/partial resection group was significantly higher than that in the total resection group or STR group.

In their Discussion, the authors considered that “the rate of deficits or complications registered in partial or subtotal resection was higher, suggesting that persistence of tumors in the surgical cavity may expose the patient to immediate or delayed complications.” However, this aggressive approach (STR) is not without a significant risk of neurological loss due to potential damage to important cortical or subcortical tissues.3 However, there is short-term protection from immediate or delayed complications with partial or subtotal resection, suggesting that there is short-term protection of the patient’s neurological function, which may be impaired in the long term.

These limitations are enlightening in and of themselves. The concept of STR is still an interesting hypothesis, but more rigorous randomized controlled trials are needed to verify the safety and effectiveness of STR in LGG. Therefore, we propose that supramaximal tumor resection based on neurological function should be considered as the treatment concept for LGGs.

Disclosures

The authors report no conflict of interest.

References

  • 1

    Rossi M, Ambrogi F, Gay L, Is supratotal resection achievable in low-grade gliomas? Feasibility, putative factors, safety, and functional outcome. J Neurosurg. 2020;132(6):16921705.

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  • 2

    Yordanova YN, Moritz-Gasser S, Duffau H. Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. J Neurosurg. 2011;115(2):232239.

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  • 3

    de Leeuw CN, Vogelbaum MA. Supratotal resection in glioma: a systematic review. Neuro Oncol. 2019;21(2):179188.

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  • Università degli Studi di Milano, Milan, Italy
Keywords:

Response

We really appreciated Mr. Wang and Dr. Chen’s Letter to the Editor about our paper, and we would like to thank them for their interest. We agree with the authors that the definition of STR may be controversial. At the moment, there is no consensus on the definition of STR in LGGs. The initial and largely accepted definition of STR is that proposed by Professor Duffau,1 which we adopted in our work: complete resection of the MRI (FLAIR)–visible tumor, with the resection cavity larger than the preoperative tumor volume. This is a “radiological” definition based on an evaluation of the extent of resection (EOR) on postoperative MRI. As a matter of fact, according to European Association of Neuro-Oncology (EANO) guidelines, an “oncological” complete resection of an LLG is defined as complete resection of a FLAIR-visible tumor mass, as evaluated on postoperative MRI.2,3 Consequently, in current neurooncological practice, the evaluation of EOR is radiological, and according to current practice, the definition of STR should be based on imaging evaluation as well. We absolutely agree that the radiological definition does not reflect the highly infiltrative nature of gliomas and of LLGs in particular. Unlike in other types of cancer, gastrointestinal, for instance, the evaluation of the cancer cell–free border to establish the limits of resection during the procedure is not a practice in neurooncological surgery. We agree with the authors that this may be the way to go in future neurooncological surgery, to reduce the gap between the current radiological definition of EOR and the “biological” one. Given these considerations, the aim of our paper was to show that pursuing a radiological STR for LGG in current practice is feasible and safe. Starting from the radiological definition, a complete resection is defined as the “absence of any signal abnormalities on postoperative MRI.” Such measurement is generally recommended on the 2-month postoperative MRI, on which most of the signal abnormalities due to small bleeding or tissue or hemostatic debris have usually disappeared.

We agree with the authors that bleeding or ischemia is the most relevant factor influencing functional outcome in glioma patients who have undergone surgery with the aid of brain mapping techniques. It is generally recommended to adopt a strict subpial resection technique, to dissect the tumor from minor or major vessels, and to limit as much as possible the use of coagulation. These surgical tips may reduce the incidence of ischemic insult and ischemia-related deficits.

Mr. Wang and Dr. Chen may be right regarding the slightly higher percentage of insular locations (34.7%) in the subtotal/partial resection group in comparison to the other resection groups (18.6% in total resection group and 16.6% in the STR group), partially explaining the higher incidence of postoperative neurological deficit recorded in this group. Interestingly, in the subtotal/partial group we also documented a higher (although not significant) incidence of perioperative complications (1.6% vs <1%). The interaction of these two variables may explain the higher postoperative morbidity in the partial resection group. Interestingly, when all variables were analyzed together in the multivariate analysis, partial/subtotal resection was associated with a higher incidence of complications.

Regarding the association between postoperative permanent deficits and EOR, when a functional neurooncological approach is used to pursue the resection, the incidence of deficits does not correlate with the location of functional boundaries, but instead with the appearance of ischemic insult. Therefore, the assumption of the larger the resection, the higher the incidence of deficits is misleading. Perhaps patients in whom a partial or subtotal resection is achieved are those harboring more complicated tumors, exposing the patients to a higher rate of complications.

Nevertheless, we agree with the authors that the currently available armamentarium to evaluate the functional impact of surgery (independent of any EOR) is still limited and that more sophisticated neuropsychological testing should be implemented.

We agree with the authors that STR in LLGs is a very interesting hypothesis. Our paper shows that when a functional neurooncological approach is applied in each patient, without any patient or tumor “a priori” selection, a radiological STR can be achieved in at least one-third of cases in a highly safe manner. The proposal for a randomized trial to assess the oncological impact is of interest, but unlike with IDH wild-type tumors, such a study should cover the long natural history of the disease and the issue of the very long accrual needed for this rare type of tumor, which, in addition to relevant ethical issues, limits the study’s feasibility.

References

  • 1

    Yordanova YN, Moritz-Gasser S, Duffau H. Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. J Neurosurg. 2011;115(2):232239.

    • Search Google Scholar
    • Export Citation
  • 2

    Schiff D, Van Den Bent M, Vogelbaum MA, Recent developments and future directions in adult lower-grade gliomas: Society for Neuro-Oncology (SNO) and European Association of Neuro-Oncology (EANO) consensus. Neuro Oncol. 2019;21(7):837853.

    • Search Google Scholar
    • Export Citation
  • 3

    Weller M, van den Bent M, Tonn JC, European Association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol. 2017;18(6):e315e329.

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    • Export Citation

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Contributor Notes

Correspondence Jincao Chen: chenjincao@hotmail.com.

INCLUDE WHEN CITING Published online August 28, 2020; DOI: 10.3171/2020.7.JNS202601.

Disclosures The authors report no conflict of interest.

  • 1

    Rossi M, Ambrogi F, Gay L, Is supratotal resection achievable in low-grade gliomas? Feasibility, putative factors, safety, and functional outcome. J Neurosurg. 2020;132(6):16921705.

    • Search Google Scholar
    • Export Citation
  • 2

    Yordanova YN, Moritz-Gasser S, Duffau H. Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. J Neurosurg. 2011;115(2):232239.

    • Search Google Scholar
    • Export Citation
  • 3

    de Leeuw CN, Vogelbaum MA. Supratotal resection in glioma: a systematic review. Neuro Oncol. 2019;21(2):179188.

  • 1

    Yordanova YN, Moritz-Gasser S, Duffau H. Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. J Neurosurg. 2011;115(2):232239.

    • Search Google Scholar
    • Export Citation
  • 2

    Schiff D, Van Den Bent M, Vogelbaum MA, Recent developments and future directions in adult lower-grade gliomas: Society for Neuro-Oncology (SNO) and European Association of Neuro-Oncology (EANO) consensus. Neuro Oncol. 2019;21(7):837853.

    • Search Google Scholar
    • Export Citation
  • 3

    Weller M, van den Bent M, Tonn JC, European Association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol. 2017;18(6):e315e329.

    • Search Google Scholar
    • Export Citation

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