5ALA in pediatric brain tumors is not routinely beneficial
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- Doris Geraldine Hines
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1 DOI.7/s ORIGINAL PER ALA in pediatric brain tumors is not routinely beneficial Jonathan Roth & Shlomi Constantini Received: 6 June 6 /Accepted: 8 February 7 # Springer-Verlag Berlin Heidelberg 7 Abstract Purpose Over recent years, -aminoluvolinic acid (ALA) has been increasingly used for resection guidance in adult high-grade gliomas. However, amongst pediatric patients, publication of intraoperative fluorescence has been limited, with inconsistent outcomes. We describe our experience and intraoperative finding amongst children with various brain tumors that were given ALA prior to tumor resection. Methods Since October, data regarding intraoperative findings amongst children that received ALA prior to tumor resection were prospectively collected. Inclusion criteria included any intracranial tumor amongst children 8 years of age. Data included intraoperative findings (regarding fluorescence of the tumor), as well as postoperative follow-up and documentation of complications. Results Fourteen children were included, covering a wide pathological spectrum: pilocytic astrocytoma () (6), medulloblastoma (), and one each of DNET, hemangiopericytoma, hemangioblastoma, ganglioneuroblastoma, oligodendroglioma grade II (OD), and ganglioglioma grade I. Fluorescence was clearly visible in one case (), and in a heterogeneous and slighter degree in two (, OD). One patient had a rash, fever, and leukocytosis 6 days after surgery and died month later from extensive tumor progression (large cell medulloblastoma with leptomeningeal spread). Conclusion ALA showed a low rate of fluorescence amongst this pediatric brain tumor cohort. These findings are consistent * Jonathan Roth jonaroth@gmail.com Department of Pediatric Neurosurgery, Dana Children s Hospital, Tel Aviv Medical Center, Tel Aviv University, 6 Weizman Street, 69 Tel Aviv, Israel with the literature, where the role of ALA in guidance of pediatric brain tumor resection is limited mainly to glioblastoma multiforme. This stems not only from the low rate of significant fluorescence, but also from inherent structural properties of these lesions such as color, consistency, and invasion. Keywords ALA. Fluorescence. Pediatric. Brain tumor Introduction Tumor resection plays an important role in many pediatric brain tumors, low as well as high-grade. For low-grade tumors, such as ependymomas, pilocytic astrocytomas, and many others, long-term survival and progression-free survival are closely linked to the ability to achieve a complete resection. Malignant tumors such as medulloblastomas and pediatric glioblastoma multiforme () are primarily treated by resection, aimed at achieving a maximally safe gross total or near gross total resection. Thus, for most types of tumor pathologies, the first line of attack is to intraoperatively identify and resect the complete tumor. Gliomas are the leading adult primary brain tumors. Over recent years, several publications have demonstrated the role of -aminoluvolinic acid (ALA) guided resection of highgrade gliomas, and its superiority over regular, white-light microscopic guided removal [ ]. Briefly, ALA is a natural intermediate substance that is converted to protoporphyrin IX (PpIX) in the mitochondria of human cells as part of the hemeporphyrin synthesis process. In certain tumors, probably due to a reduction of the enzyme ferrochelatase (that converts the PpIX to heme), following external admission of ALA, PpIX accumulates in the mitochondria. When tissue is excited by a light at a wavelength of 7 nm, the PpIX fluorescents (FL) at a wavelength of about 6 nm. This FL assists to
2 distinguish the pathological tissue from the surrounding nontumoral tissue. The implications of an intraoperative tumor-specific marker for pediatric brain tumor surgery has motivated many medical centers, including our own, to explore the efficacy and safety of ALA usage in pediatric brain tumor surgery. In this manuscript, we share our local experience, as well as review the literature of ALA use in children. Methods Following institutional review board (IRB) approval, a prospective, open-label, non-randomized, phase II study was conducted. Patients were included if they were between and 8 years of age at the time of surgery, or if their tumor was known to be present prior to the age of 8 ( patient). Inclusion criteria included parental consent, intra-axial brain tumor, and liver and renal function up to twice the upper normal limit. Exclusion criteria included any first-degree relative with porphyria, any known hepatic disease within the preceding year, any known cutaneous hypersensitivity, or an inability to fulfill safety measures. Safety measures included avoidance of direct sunlight exposure for 8 h following ALA admission. Study protocol Following parental consent, and completion of baseline hepatic and renal function studies, a single dose of ALA was administered orally at the dosage of mg/kg, suspended in cm of tap water. The drug was administered 6 h preoperatively. At surgery, following tumor exposure, the microscope (Zeiss, OPMI, Pentero 9) was used to evaluate for fluorescence. Tumor resection was performed using regular surgical techniques. Tumor resection was guided by regular tissue appearance under the white microscopic light. Intermittently during resection, fluorescence was evaluated, rated as negative, positive, or heterogeneous. Following surgery, the child was kept in the ICU and then in the department, with no direct sunlight exposure for at least 8 h. CBC, liver functions, and AED levels were monitored daily for at least days. Patient data, including any side effects and tumor fluorescence, were prospectively collected. Statistics and data analysis As the number of patients was small, data presentation is mostly descriptive, including mean ± standard deviation. Results Between October and May 6, children were recruited for the study. This represents about % of all pediatric brain tumors operated during this time frame. The sole reason for which eligible children were not included in the study was parental refusal. Ages at surgery were 9 years of age ( ± ). Tumor pathology and location were heterogeneous, including pilocytic astrocytoma (6), medulloblastoma (), ganglioneuroblastoma (), ganglioglioma grade I (), hemangioblastoma (), hemangiopericytoma (), oligodendroglioma grade II (), and dysembryoplastic neuroepithelial tumor (DNET, ). Tumor location included posterior fossa (8), frontal lobe (), temporal lobe (), and thalamic-basal ganglia (). ALA was administered. 6 h (. ±.8) prior to tumor exposure. Fluorescence of children had negative fluorescence. One had a positive fluorescence (pilocytic astrocytoma, Fig. ), and two had heterogeneous fluorescence (one pilocytic astrocytoma, and one oligodendroglioma grade II, Figs. ). As the numbers of each pathology were small, no meaningful statistics could be applied. However, of the most common pathology (pilocytic astrocytoma, six cases), four had negative fluorescence, one was positive, and one heterogeneous. Complications There was one complication. A -year-old girl presented with a posterior fossa tumor and leptomeningeal spread. She received ALA as per protocol and underwent a resection of what eventually proved to be a large-cell medulloblastoma. She was not exposed to direct sunlight for several days after surgery. Six days following surgery, she developed a diffuse rash, fever, and leukocytosis of about,. She underwent an extensive work up, excluding any infection. Liver functions were within normal range. Results of a skin biopsy were compatible with contact dermatitis. She developed hydrocephalus and underwent shunt surgery. One month after the primary surgery, she deteriorated secondary to massive tumor progression and underwent partial tumor debulking. Unfortunately, she died within days. Literature review To date, cases applying ALA in pediatric brain tumors have been published (Table )[ ]. Most publications have included only a handful of cases. Even the larger series published were formed by combining data from several centers (each contributing a small number of patients) and composed of a heterogeneous pathological group. Most publications
3 Childs Nerv Syst Fig. An 8 year old with an exophytic brainstem pilocytic astrocytoma. Intraoperative figures show the surgical bed under regular white light (above) and during fluorescence (bellow). The tumor showed clear and heterogeneous FL have used the same dose ( mg/kg, similar to adults), administered several hours prior to surgery (usually between and 6 h). Combining all published data concerning ALA use for resection of pediatric brain tumors including the current series, several larger sub-groups can be identified: pilocytic astrocytomas (, cases), glioblastoma multiforme (, cases), medulloblstomas (, cases), and anaplastic ependymomas (AE, cases). The remaining pathologies number less than each. Amongst the larger groups, fluorescence was avid in % of, 86% of, 8% of, and % of AE. In each group, certain patients had a heterogeneous, fainter fluorescence, visible in % of the, % of, % of, and Fig. An extensive frontal pilocytic astrocytoma in a 7 year old. Intraoperative figure shows mild and heterogeneous FL % of AE. Of the smaller pathological groups, fluorescence was positive in / sarcomas, /8 supratentorial PNET, / PXA, / AO, / meningioma, /8 GG grade I, / ependymoma grade II, / DA grade II, and /6 AA. Discussion ALA plays an important role in resection of high-grade gliomas in adults. Intraoperative identification of tumor regions, indicated through fluorescence, guides the surgeon to resect tumoral tissue that would otherwise not be identified as such under regular white light. A prospective phase III study
4 Childs Nerv Syst Fig. A right frontal oligodendroglioma grade II in a 9 year old. Intraoperative figure shows heterogeneous FL Table Summary of pediatric cases and the fluorescence outcome Publication Pathology Total number of cases Barbagallo [] AA AE Sarcoma DA II Supratentorial PNET AE GG I NB PXA AA AE Supratentorial PNET GG Ep II Oligo II Oligo III DNET PXA DA II Glioneural ACPP Meningioma Lipoma Neuroblastoma Sarcoma Gliotic tissue DNET Ganglioneuroblastoma Hemangioblastoma Hemangiopericytoma Oligo II GG II Beez [] Bernal Garcia [6] Eicker [7] Moriuchi [8] Preuβ [9] Ruge [] Skjøth-Rasmussen [] Stummer [] Current study Number of heterogeneous FL Number of positive FL AA anaplastic astrocytoma, ACPP atypical choroid plexus papilloma, AE anaplastic ependymoma, DA diffuse astrocytoma, Ep ependymoma, glioblastoma multiforme, PXA pleomorphic xanthoastrocytoma
5 demonstrated a positive impact on progression-free survival when resection is guided by ALA fluorescence as compared to resection performed under regular microscope white light []. Despite these advantages in adult surgery, its role in guiding tumor resection in pediatric brain tumors seems to be limited. Similar to the adult population, most pediatric show a positive FL following ALA admission. However, this pathological entity is relatively rare in children, comprising only about % of all primary pediatric brain tumors []. Aside from the group, most other pathologies show limited FL. The reasons for the discrepancy between various types of pediatric tumors, including in the high-grade tumor groups (such as ), are unclear. One possible explanation may be the differences in the mitochondrial enzyme ferrochelatase. This enzyme is thought to be downregulated in adult cells, thus increasing the level of intracellular PpIX that emits the fluorescence. Using ALA during pediatric brain tumor resection needs to be evaluated not only on the basis of the sensitivity of FL per specific pathology but also at a wider perspective. Most pediatric brain tumors differ from adult high-grade gliomas in several aspects: tumor consistency and appearance usually differ from the surrounding brain. This is true for grade I astrocytomas (), medulloblastomas, and ependymomas. The pediatric tumors usually do not infiltrate the adjacent brain tissue to a significant degree, and thus differentiating between the tumor and the brain is more straightforward as opposed to adult glioma surgery. These structural differences enable a more extensive resection in most pediatric brain tumors using regular microscope light and surgeon judgment. All this said, and in view of the above results regarding the low sensitivity of ALA in many of the pediatric tumors, there is probably a limited and selective role for the use of ALA in pediatric brain tumor resection. The complication rate of ALA in children is extremely low. It was noted that some children displayed up to a -fold increase in transaminases []. This is a well-known phenomenon in adults receiving ALA, and it gradually decreases over the course of a few days. No other ALA complications have been described in the pediatric literature, including rashes. Thus, our single case of complications of a fulminant rash, fevers, and leukocytosis is an exception to the known literature. Following exclusion of other possible causes (mainly infection), we have no explanation for this complication s occurrence. We did not find any other published case (child or adult) with a leptomeningeal disease that received ALA. We did not find any other instances of such complications amongst the many papers describing ALA use in the adult population. As ALA is a natural metabolite that is metabolized within hours, we assume that complications occurring 6 days following drug admission (without any other metabolic abnormalities) are not associated with the ALA. Limitations The literature relating to ALA use in pediatric brain tumor resection originates in many different institutions with a wide range of inclusion and exclusion criteria, dealing with a very heterogeneous pathology group. Additionally, the WHO has recently published a new tumor classification []. We could not comment on the current classification of cases published in prior series; however, in the current series, most pathologies (e.g., pilocytic astrocytoma) would not differ in the new WHO classification. Future studies should reevaluate the use of ALA according to the new classification. Quantifying fluorescence levels is subjective, ill defined, and suffers from intra-observer, inter-observer, and interinstitutional inconsistencies. BSlight/heterogeneous^ FL may be seen in non-tumoral lesions such as gliotic tissue and lipomas (Table ) or peritumoral and non-invaded brain [ 9]. Thus, appearances that seem to differentiate tumor from noninfiltrated brain or non-tumoral tissue may be deceptive. This phenomenon is known in the adult literature; however, the implication in the pediatric pathology spectrum is unknown. In addition, steroids and AED (especially phenytoin) may affect ALA uptake and various tumor and steroid protocols may influence the results []. Another factor differing children and adults may be differences in drug metabolism, possibly affecting pharmacodynamics. Thus, perhaps the time lag between drug admission and actual intraoperative fluorescence evaluation could differ between children and adults. Conclusions Currently, ALA seems to play a limited role in pediatric brain tumor resection and is not routinely recommended. Some exceptions to this include, for which ALA commonly leads to fluorescence, and lesions invading deep/critical structures for which an additional tool differentiating tumor from brain is advantageous. Acknowledgments We thank Mrs. Adina Sherer for editing assistance, and Mrs. Sigal Freedman for graphical assistance. Compliance with ethical standards Conflict of interest interest. References The authors declare that they have no conflict of. Stummer W, Stocker S, Novotny A, Heimann A, Sauer O, Kempski O, Plesnila N, Wietzorrek J, Reulen HJ (998) In vitro and in vivo porphyrin accumulation by C6 glioma cells after exposure to - aminolevulinic acid. J Photochem Photobiol B :6 69
6 . Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ () Fluorescence-guided resection of glioblastoma multiforme by using -aminolevulinic acid-induced porphyrins: a prospective study in consecutive patients. J Neurosurg 9:. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ (6) Fluorescence-guided surgery with - aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7: 9. Barbagallo GM, Certo F, Heiss K, Albanese V () -ALA fluorescence-assisted surgery in pediatric brain tumors: report of three cases and review of the literature. Br J Neurosurg 8(6):7 7. Beez T, Sarikaya-Seiwert S, Steiger HJ, Hanggi D () Fluorescence-guided surgery with -aminolevulinic acid for resection of brain tumors in children a technical report. Acta Neurochir 6: Bernal Garcia LM, Cabezudo Artero JM, Royano Sanchez M, Marcelo Zamorano, Lopez Macias M () Fluorescenceguided resection with -aminolevulinic acid of meningeal sarcoma in a child. Child s nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery : Eicker S, Sarikaya-Seiwert S, Borkhardt A, Gierga K, Turowski B, Heiroth HJ, Steiger HJ, Stummer W () ALA-induced porphyrin accumulation in medulloblastoma and its use for fluorescenceguided surgery. Cent Eur Neurosurg 7: 8. Moriuchi S, Yamada K, Dehara M, Teramoto Y, Soda T, Imakita M, Taneda M () Use of -aminolevulinic acid for the confirmation of deep-seated brain tumors during stereotactic biopsy. Report of cases. J Neurosurg : Preuss M, Renner C, Krupp W, Christiansen H, Fischer L, Merkenschlager A, Kiess W, Muller W, Manzo N, Meixensberger J, Nestler U () The use of -aminolevulinic acid fluorescence guidance in resection of pediatric brain tumors. Child s nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery 9:6 67. Ruge JR, Liu J (9) Use of -aminolevulinic acid for visualization and resection of a benign pediatric brain tumor. J Neurosurg Pediatr :8 86. Skjoth-Rasmussen J, Bogeskov L, Sehested A, Klausen C, Broholm H, Nysom K () The use of -ALA to assist complete removal of residual non-enhancing part of childhood medulloblastoma: a case report. Child s nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery :7 77. Stummer W, Rodrigues F, Schucht P, Preuss M, Wiewrodt D, Nestler U, Stein M, Artero JM, Platania N, Skjoth-Rasmussen J, Della Puppa A, Caird J, Cortnum S, Eljamel S, Ewald C, Gonzalez- Garcia L, Martin AJ, Melada A, Peraud A, Brentrup A, Santarius T, Steiner HH, European ALAPBTSG () Predicting the Busefulness^ of -ALA-derived tumor fluorescence for fluorescence-guided resections in pediatric brain tumors: a European survey. Acta Neurochir 6:. Ostrom QT, de Blank PM, Kruchko C, Petersen CM, Liao P, Finlay JL, Stearns DS, Wolff JE, Wolinsky Y, Letterio JJ, Barnholtz-Sloan JS () Alex s lemonade stand foundation infant and childhood primary brain and central nervous system tumors diagnosed in the United States in 7. Neuro-Oncology 6(Suppl ):x x6. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella- Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (6) The 6 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol :8 8. Kamp MA, Grosser P, Felsberg J, Slotty PJ, Steiger HJ, Reifenberger G, Sabel M () -aminolevulinic acid (-ALA)- induced fluorescence in intracerebral metastases: a retrospective study. Acta Neurochir : 8 discussion 8 6. Novotny A, Xiang J, Stummer W, Teuscher NS, Smith DE, Keep RF () Mechanisms of -aminolevulinic acid uptake at the choroid plexus. J Neurochem 7: 8 7. Schucht P, Beck J, Vajtai I, Raabe A () Paradoxical fluorescence after administration of -aminolevulinic acid for resection of a cerebral melanoma metastasis. Acta Neurochir : Utsuki S, Miyoshi N, Oka H, Miyajima Y, Shimizu S, Suzuki S, Fujii K (7a) Fluorescence-guided resection of metastatic brain tumors using a -aminolevulinic acid-induced protoporphyrin IX: pathological study. Brain Tumor Pathol : 9. UtsukiS,OkaH,SatoS,ShimizuS,SuzukiS,TanizakiY, Kondo K, Miyajima Y, Fujii K (7b) Histological examination of false positive tissue resection using - aminolevulinic acid-induced fluorescence guidance. Neurol Med Chir 7: discussion -. Hefti M, Albert I, Luginbuehl V () Phenytoin reduces - aminolevulinic acid-induced protoporphyrin IX accumulation in malignant glioma cells. J Neuro-Oncol 8:
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