Skip to main content
Top
Published in: Acta Neurochirurgica 5/2019

01-05-2019 | Meningioma | Original Article - Tumor - Meningioma

Fluorescence imaging of meningioma cells with somatostatin receptor ligands: an in vitro study

Authors: Stefan Linsler, Ralf Ketter, Joachim Oertel, Steffi Urbschat

Published in: Acta Neurochirurgica | Issue 5/2019

Login to get access

Abstract

Background

The use of five-aminolevulinic acid (5-ALA) in the staining of malignant glioma cells has significantly improved intraoperative radicality in the resection of gliomas in the last decade. Currently, there is no comparable selective fluorescent substance available for meningiomas. There is however a demand for intraoperative fluorescent identification of, e.g., invasive skull base meningiomas to help improve safe radical resection. Meningiomas show high expression of the somatostatin receptor type 2, offering the possibility of receptor-targeted imaging. The authors used a somatostatin receptor-labeled fluorescence dye in the identification of meningiomas in vitro. The aim of this study was to evaluate the possibility of selective identification of meningioma cells with fluorescent techniques.

Methods

Twenty-four primary human meningioma cell cultures were analyzed. The tumor cells were incubated with FAM-TOC (5,6-Carboxyfluoresceine-Tyr3-Octreotide). As a negative control, four human dura tissues were cultured as well as a mixed cell culture in vitro and incubated with the same somatostatin receptor-labeled fluorescence substance. After incubation, fluorescence signal and intensity in all cell cultures were analyzed at three different time points using a fluorescence microscope with 488 nm epi-illumination.

Results

Sixteen WHO I, six WHO II, two WHO III meningioma primary cell cultures, and four dura cell cultures were analyzed. Fluorescence was detected in all meningioma cell cultures (22 cell culture stained strongly, 2 cell cultures moderately) directly after incubation up until 4 h later. There were no differences in the quality and quantity of fluorescence signal between the various meningioma grades. The fluorescence signal persisted unchanged during the analyzed period. In the negative control, dura cell cultures remained unstained.

Conclusions

This study demonstrates the use of FAM-TOC in the selective fluorescent identification of meningioma cells in vitro. Further evaluation of the chemical kinetics of the applied somatostatin receptor ligand and fluorescence dye is warranted. As a next step, an experimental animal model is needed to evaluate these promising results in vivo.
Literature
1.
go back to reference Akcakaya MO, Goker B, Kasimcan MO, Hamamcioglu MK, Kiris T (2017) Use of sodium fluorescein in meningioma surgery performed under the YELLOW-560 nm surgical microscope filter: feasibility and preliminary results. World Neurosurg 107:966–973CrossRefPubMed Akcakaya MO, Goker B, Kasimcan MO, Hamamcioglu MK, Kiris T (2017) Use of sodium fluorescein in meningioma surgery performed under the YELLOW-560 nm surgical microscope filter: feasibility and preliminary results. World Neurosurg 107:966–973CrossRefPubMed
2.
go back to reference Bedwell J, MacRobert AJ, Phillips D, Bown SG (1992) Fluorescence distribution and photodynamic effect of ALA-induced PP IX in the DMH rat colonic tumour model. Br J Cancer 65:818–824CrossRefPubMedPubMedCentral Bedwell J, MacRobert AJ, Phillips D, Bown SG (1992) Fluorescence distribution and photodynamic effect of ALA-induced PP IX in the DMH rat colonic tumour model. Br J Cancer 65:818–824CrossRefPubMedPubMedCentral
3.
go back to reference Beks JW, de Windt HL (1988) The recurrence of supratentorial meningiomas after surgery. Acta Neurochir 95:3–5CrossRefPubMed Beks JW, de Windt HL (1988) The recurrence of supratentorial meningiomas after surgery. Acta Neurochir 95:3–5CrossRefPubMed
4.
go back to reference Borovich B, Doron Y (1986) Recurrence of intracranial meningiomas: the role played by regional multicentricity. J Neurosurg 64:58–63CrossRefPubMed Borovich B, Doron Y (1986) Recurrence of intracranial meningiomas: the role played by regional multicentricity. J Neurosurg 64:58–63CrossRefPubMed
5.
go back to reference Borovich B, Doron Y, Braun J, Guilburd JN, Zaaroor M, Goldsher D, Lemberger A, Gruszkiewicz J, Feinsod M (1986) Recurrence of intracranial meningiomas: the role played by regional multicentricity. Part 2: clinical and radiological aspects. J Neurosurg 65:168–171CrossRefPubMed Borovich B, Doron Y, Braun J, Guilburd JN, Zaaroor M, Goldsher D, Lemberger A, Gruszkiewicz J, Feinsod M (1986) Recurrence of intracranial meningiomas: the role played by regional multicentricity. Part 2: clinical and radiological aspects. J Neurosurg 65:168–171CrossRefPubMed
6.
go back to reference da Silva CE, Peixoto de Freitas PE (2016) Recurrence of skull base meningiomas: the role of aggressive removal in surgical treatment. J Neurol Surg B Skull Base 77:219–225PubMed da Silva CE, Peixoto de Freitas PE (2016) Recurrence of skull base meningiomas: the role of aggressive removal in surgical treatment. J Neurol Surg B Skull Base 77:219–225PubMed
8.
go back to reference Ding D, Starke RM, Hantzmon J, Yen CP, Williams BJ, Sheehan JP (2013) The role of radiosurgery in the management of WHO Grade II and III intracranial meningiomas. Neurosurg Focus 35:E16CrossRefPubMed Ding D, Starke RM, Hantzmon J, Yen CP, Williams BJ, Sheehan JP (2013) The role of radiosurgery in the management of WHO Grade II and III intracranial meningiomas. Neurosurg Focus 35:E16CrossRefPubMed
9.
go back to reference Graillon T, Romano D, Defilles C, Saveanu A, Mohamed A, Figarella-Branger D, Roche PH, Fuentes S, Chinot O, Dufour H, Barlier A (2017) Octreotide therapy in meningiomas: in vitro study, clinical correlation, and literature review. J Neurosurg 127:660–669CrossRefPubMed Graillon T, Romano D, Defilles C, Saveanu A, Mohamed A, Figarella-Branger D, Roche PH, Fuentes S, Chinot O, Dufour H, Barlier A (2017) Octreotide therapy in meningiomas: in vitro study, clinical correlation, and literature review. J Neurosurg 127:660–669CrossRefPubMed
10.
go back to reference Hellwig D, Samnick S, Reif J, Romeike BF, Reith W, Moringlane JR, Kirsch CM (2002) Comparison of tc-99m depreotide and in-111 octreotide in recurrent meningioma. Clin Nucl Med 27:781–784CrossRefPubMed Hellwig D, Samnick S, Reif J, Romeike BF, Reith W, Moringlane JR, Kirsch CM (2002) Comparison of tc-99m depreotide and in-111 octreotide in recurrent meningioma. Clin Nucl Med 27:781–784CrossRefPubMed
11.
go back to reference Henn W, Cremerius U, Heide G, Lippitz B, Schroder JM, Gilsbach JM, Bull U, Zang KD (1995) Monosomy 1p is correlated with enhanced in vivo glucose metabolism in meningiomas. Cancer Genet Cytogenet 79:144–148CrossRefPubMed Henn W, Cremerius U, Heide G, Lippitz B, Schroder JM, Gilsbach JM, Bull U, Zang KD (1995) Monosomy 1p is correlated with enhanced in vivo glucose metabolism in meningiomas. Cancer Genet Cytogenet 79:144–148CrossRefPubMed
12.
go back to reference Kamp MA, Fischer I, Buhner J, Turowski B, Cornelius JF, Steiger HJ, Rapp M, Slotty PJ, Sabel M (2016) 5-ALA fluorescence of cerebral metastases and its impact for the local-in-brain progression. Oncotarget 7:66776–66789CrossRefPubMedPubMedCentral Kamp MA, Fischer I, Buhner J, Turowski B, Cornelius JF, Steiger HJ, Rapp M, Slotty PJ, Sabel M (2016) 5-ALA fluorescence of cerebral metastases and its impact for the local-in-brain progression. Oncotarget 7:66776–66789CrossRefPubMedPubMedCentral
13.
go back to reference Kawahara Y, Niiro M, Yokoyama S, Kuratsu J (2001) Dural congestion accompanying meningioma invasion into vessels: the dural tail sign. Neuroradiology 43:462–465CrossRefPubMed Kawahara Y, Niiro M, Yokoyama S, Kuratsu J (2001) Dural congestion accompanying meningioma invasion into vessels: the dural tail sign. Neuroradiology 43:462–465CrossRefPubMed
14.
go back to reference Ketter R, Kim YJ, Storck S, Rahnenfuhrer J, Romeike BF, Steudel WI, Zang KD, Henn W (2007) Hyperdiploidy defines a distinct cytogenetic entity of meningiomas. J Neuro-Oncol 83:213–221CrossRef Ketter R, Kim YJ, Storck S, Rahnenfuhrer J, Romeike BF, Steudel WI, Zang KD, Henn W (2007) Hyperdiploidy defines a distinct cytogenetic entity of meningiomas. J Neuro-Oncol 83:213–221CrossRef
15.
go back to reference Ketter R, Urbschat S, Henn W, Feiden W, Beerenwinkel N, Lengauer T, Steudel WI, Zang KD, Rahnenfuhrer J (2007) Application of oncogenetic trees mixtures as a biostatistical model of the clonal cytogenetic evolution of meningiomas. Int J Cancer 121:1473–1480CrossRefPubMed Ketter R, Urbschat S, Henn W, Feiden W, Beerenwinkel N, Lengauer T, Steudel WI, Zang KD, Rahnenfuhrer J (2007) Application of oncogenetic trees mixtures as a biostatistical model of the clonal cytogenetic evolution of meningiomas. Int J Cancer 121:1473–1480CrossRefPubMed
16.
go back to reference Ketter R, Rahnenfuhrer J, Henn W, Kim YJ, Feiden W, Steudel WI, Zang KD, Urbschat S (2008) Correspondence of tumor localization with tumor recurrence and cytogenetic progression in meningiomas. Neurosurgery 62:61–69 discussion 69-70CrossRefPubMed Ketter R, Rahnenfuhrer J, Henn W, Kim YJ, Feiden W, Steudel WI, Zang KD, Urbschat S (2008) Correspondence of tumor localization with tumor recurrence and cytogenetic progression in meningiomas. Neurosurgery 62:61–69 discussion 69-70CrossRefPubMed
17.
go back to reference Knipps J, Beseoglu K, Kamp M, Fischer I, Felsberg J, Neumann LM, Steiger HJ, Cornelius JF (2017) Fluorescence behavior and dural infiltration of meningioma analyzed by 5-aminolevulinic acid-based fluorescence: operating microscope versus mini-spectrometer. World Neurosurg 108:118–127CrossRefPubMed Knipps J, Beseoglu K, Kamp M, Fischer I, Felsberg J, Neumann LM, Steiger HJ, Cornelius JF (2017) Fluorescence behavior and dural infiltration of meningioma analyzed by 5-aminolevulinic acid-based fluorescence: operating microscope versus mini-spectrometer. World Neurosurg 108:118–127CrossRefPubMed
18.
go back to reference Linsler S, Kraemer D, Driess C, Oertel J, Kammers K, Rahnenfuhrer J, Ketter R, Urbschat S (2014) Molecular biological determinations of meningioma progression and recurrence. PLoS One 9:e94987CrossRefPubMedPubMedCentral Linsler S, Kraemer D, Driess C, Oertel J, Kammers K, Rahnenfuhrer J, Ketter R, Urbschat S (2014) Molecular biological determinations of meningioma progression and recurrence. PLoS One 9:e94987CrossRefPubMedPubMedCentral
19.
go back to reference Linsler S, Keller C, Urbschat S, Ketter R, Oertel J (2016) Prognosis of meningiomas in the early 1970s and today. Clin Neurol Neurosurg 149:98–103CrossRefPubMed Linsler S, Keller C, Urbschat S, Ketter R, Oertel J (2016) Prognosis of meningiomas in the early 1970s and today. Clin Neurol Neurosurg 149:98–103CrossRefPubMed
20.
go back to reference Linsler S, Fischer G, Skliarenko V, Stadie A, Oertel J (2017) Endoscopic assisted supraorbital keyhole approach or endoscopic endonasal approach in case of tuberculum sellae meningioma: which surgical route should be favoured? World Neurosurg 104:601–611CrossRefPubMed Linsler S, Fischer G, Skliarenko V, Stadie A, Oertel J (2017) Endoscopic assisted supraorbital keyhole approach or endoscopic endonasal approach in case of tuberculum sellae meningioma: which surgical route should be favoured? World Neurosurg 104:601–611CrossRefPubMed
21.
go back to reference Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109CrossRefPubMedPubMedCentral Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109CrossRefPubMedPubMedCentral
22.
go back to reference Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820CrossRefPubMed Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820CrossRefPubMed
23.
go back to reference Millesi M, Kiesel B, Mischkulnig M, Martinez-Moreno M, Wohrer A, Wolfsberger S, Knosp E, Widhalm G (2016) Analysis of the surgical benefits of 5-ALA-induced fluorescence in intracranial meningiomas: experience in 204 meningiomas. J Neurosurg 125:1408–1419CrossRefPubMed Millesi M, Kiesel B, Mischkulnig M, Martinez-Moreno M, Wohrer A, Wolfsberger S, Knosp E, Widhalm G (2016) Analysis of the surgical benefits of 5-ALA-induced fluorescence in intracranial meningiomas: experience in 204 meningiomas. J Neurosurg 125:1408–1419CrossRefPubMed
24.
go back to reference Morofuji Y, Matsuo T, Hayashi Y, Suyama K, Nagata I (2008) Usefulness of intraoperative photodynamic diagnosis using 5-aminolevulinic acid for meningiomas with cranial invasion: technical case report. Neurosurgery 62:102–103 discussion 103-104PubMed Morofuji Y, Matsuo T, Hayashi Y, Suyama K, Nagata I (2008) Usefulness of intraoperative photodynamic diagnosis using 5-aminolevulinic acid for meningiomas with cranial invasion: technical case report. Neurosurgery 62:102–103 discussion 103-104PubMed
25.
go back to reference Rokni-Yazdi H, Azmoudeh Ardalan F, Asadzandi Z, Sotoudeh H, Shakiba M, Adibi A, Ayatollahi H, Rahmani M (2009) Pathologic significance of the “dural tail sign”. Eur J Radiol 70:10–16CrossRefPubMed Rokni-Yazdi H, Azmoudeh Ardalan F, Asadzandi Z, Sotoudeh H, Shakiba M, Adibi A, Ayatollahi H, Rahmani M (2009) Pathologic significance of the “dural tail sign”. Eur J Radiol 70:10–16CrossRefPubMed
26.
go back to reference Scheichel F, Ungersboeck K, Kitzwoegerer M, Marhold F (2017) Fluorescence-guided resection of extracranial soft tissue tumour infiltration in atypical meningioma. Acta Neurochir 159:1027–1031CrossRefPubMed Scheichel F, Ungersboeck K, Kitzwoegerer M, Marhold F (2017) Fluorescence-guided resection of extracranial soft tissue tumour infiltration in atypical meningioma. Acta Neurochir 159:1027–1031CrossRefPubMed
27.
go back to reference Schick B, Wolf G, Romeike BF, Mestres P, Praetorius M, Plinkert PK (2003) Dural cell culture. A new approach to study duraplasty. Cells Tissues Organs 173:129–137CrossRefPubMed Schick B, Wolf G, Romeike BF, Mestres P, Praetorius M, Plinkert PK (2003) Dural cell culture. A new approach to study duraplasty. Cells Tissues Organs 173:129–137CrossRefPubMed
28.
go back to reference Silva CB, Ongaratti BR, Trott G, Haag T, Ferreira NP, Leaes CG, Pereira-Lima JF, Oliveira Mda C (2015) Expression of somatostatin receptors (SSTR1-SSTR5) in meningiomas and its clinicopathological significance. Int J Clin Exp Pathol 8:13185–13192PubMedPubMedCentral Silva CB, Ongaratti BR, Trott G, Haag T, Ferreira NP, Leaes CG, Pereira-Lima JF, Oliveira Mda C (2015) Expression of somatostatin receptors (SSTR1-SSTR5) in meningiomas and its clinicopathological significance. Int J Clin Exp Pathol 8:13185–13192PubMedPubMedCentral
30.
go back to reference Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ (2000) Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 93:1003–1013CrossRefPubMed Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ (2000) Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 93:1003–1013CrossRefPubMed
31.
go back to reference Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ, Group AL-GS (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401CrossRefPubMed Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ, Group AL-GS (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401CrossRefPubMed
32.
go back to reference Valery CA, Faillot M, Lamproglou I, Golmard JL, Jenny C, Peyre M, Mokhtari K, Mazeron JJ, Cornu P, Kalamarides M (2016) Grade II meningiomas and Gamma Knife radiosurgery: analysis of success and failure to improve treatment paradigm. J Neurosurg 125:89–96CrossRefPubMed Valery CA, Faillot M, Lamproglou I, Golmard JL, Jenny C, Peyre M, Mokhtari K, Mazeron JJ, Cornu P, Kalamarides M (2016) Grade II meningiomas and Gamma Knife radiosurgery: analysis of success and failure to improve treatment paradigm. J Neurosurg 125:89–96CrossRefPubMed
33.
go back to reference Wohrer A, Waldhor T, Heinzl H, Hackl M, Feichtinger J, Gruber-Mosenbacher U, Kiefer A, Maier H, Motz R, Reiner-Concin A, Richling B, Idriceanu C, Scarpatetti M, Sedivy R, Bankl HC, Stiglbauer W, Preusser M, Rossler K, Hainfellner JA (2009) The Austrian Brain Tumour Registry: a cooperative way to establish a population-based brain tumour registry. J Neuro-Oncol 95:401–411CrossRef Wohrer A, Waldhor T, Heinzl H, Hackl M, Feichtinger J, Gruber-Mosenbacher U, Kiefer A, Maier H, Motz R, Reiner-Concin A, Richling B, Idriceanu C, Scarpatetti M, Sedivy R, Bankl HC, Stiglbauer W, Preusser M, Rossler K, Hainfellner JA (2009) The Austrian Brain Tumour Registry: a cooperative way to establish a population-based brain tumour registry. J Neuro-Oncol 95:401–411CrossRef
Metadata
Title
Fluorescence imaging of meningioma cells with somatostatin receptor ligands: an in vitro study
Authors
Stefan Linsler
Ralf Ketter
Joachim Oertel
Steffi Urbschat
Publication date
01-05-2019
Publisher
Springer Vienna
Published in
Acta Neurochirurgica / Issue 5/2019
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-019-03872-x

Other articles of this Issue 5/2019

Acta Neurochirurgica 5/2019 Go to the issue

Technical Note - Functional Neurosurgery - Epilepsy

Three-dimensional neuronavigation in SEEG-guided epilepsy surgery