|
|
|
|
|
|
||
|
|
||||
|
|
||||
|
||||
Clinical Neuro-Oncology |
Brain Tumor Center, Massachusetts General Hospital, Boston, MA 02114 (R.K.B., F.H.H.); National Cancer Institute, Bethesda, MD 20892 (E.F.); National Institutes of Health, Bethesda, MD 20892 (P.M.B); Department of Pharmaceutics, University of Minnesota, Minneapolis, MN 55455 (W.F.E.); St. Jude Children's Research Hospital, Memphis, TN 38105 (C.F.S.); Department of Pharmacology, Fox Chase Cancer Center, Philadelphia, PA 19111 (J.M.G.); Laboratory of Clinical Pharmacology, Center for Drug Evaluation and Research, Food and Drug Administration, Rockville, MD 20857 (J.M.C.); CMA Microdialysis, North Chelmsford, MA 01863 (R.P.P); The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030 (J.F.D.); Human Performance Laboratory, East Carolina University, Greenville, NC 27858 (R.C.H.); Psychiatry Department, Yale University, New Haven, CT 06519 (I.C.); Department of Neuro-Oncology, Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231 (S.A.G.); Department of Medicine, Duke University Medical Center, Durham, NC 27710 (O.M.C.); USA
1 Address correspondence to Ramsis K. Benjamin, Carolina Neurosurgery & Spine Associates, Neuro-Oncology Center, 1628 E. Morehead Road, Suite 200, Charlotte, NC 28207 (Ramsis.benjamin{at}cnsa.com).
Abstract
In individuals with brain tumors, pharmacodynamic and pharmacokinetic studies of therapeutic agents have historically used analyses of drug concentrations in serum or cerebrospinal fluid, which unfortunately do not necessarily reflect concentrations within the tumor and adjacent brain. This review article introduces to neurological and medical oncologists, as well as pharmacologists, the application of microdialysis in monitoring drug metabolism and delivery within the fluid of the interstitial space of brain tumor and its surroundings. Microdialysis samples soluble molecules from the extracellular fluid via a semipermeable membrane at the tip of a probe. In the past decade, it has been used predominantly in neurointensive care in the setting of brain trauma, vasospasm, epilepsy, and intracerebral hemorrhage. At the first Carolyn Frye-Halloran Symposium held at Massachusetts General Hospital in March 2002, the concept of microdialysis was extended to specifically address its possible use in treating brain tumor patients. In doing so we provide a rationale for the use of this technology by a National Cancer Institute consortium, New Approaches to Brain Tumor Therapy, to measure levels of drugs in brain tissue as part of phase 1 trials.
References
Abi-Saab, W.M., Maggs, D.G., Jones, T., Jacob, R., Srihari, V., Thompson, J., Kerr, D., Leone, P., Krystal, J.H., Spencer, D.D., During, M.J., and Sherwin, R.S. (2002) Striking differences in glucose and lactate levels between brain extracellular fluid and plasma in conscious human sub jects: Effects of hyperglycemia and hypoglycemia. J. Cereb. Blood Flow Metab. 22,271 -279.[CrossRef][ISI][Medline]
Alessandri, B., Doppenberg, E., Bullock, R., Woodward, J., Choi, S., Koura, S., and Young, H.F. (1999a) Glucose and lactate metabolism after severe human head injury: Influence of excitatory neurotransmitters and injury type. Acta Neurochir. Suppl. (Wien) 75,21 -24.
Alessandri, B., Doppenberg, E., Zauner, A., Woodward, J., Choi, S., and Bul lock, R. (1999b) Evidence for time-dependent glutamate-mediated gly colysis in head-injured patients: A microdialysis study. Acta Neurochir. Suppl. (Wien) 75, 25-28.[Medline]
Bobo, R.H., Laske, D.W., Akbasak, A., Morrison, P.F., Dedrick,
R.L., and Oldfield, E.H. (1994) Convection-enhanced delivery of
macromolecules in the brain. Proc. Nat. Acad. Sci. USA
91,2076
-2080.
Boiardi, A., Eoli, M., Pozzi, A., Salmaggi, A., Broggi, G., and Silvani, A. (1999) Locally delivered chemotherapy and repeated surgery can improve survival in glioblastoma patients. Ital. J. Neurol. Sci. 20,43 -48.[CrossRef][ISI][Medline]
Brada, M., and Shape, G. (1996) Chemotherapy of high grade gliomas: Beginning of a new era or the end of the old? Eur. J. Cancer 32A,2193 -2194 (editorial).[CrossRef]
Brada, M., and Yung, W.K. (2000) Clinical trial end points in malignant glioma: Need for effective trial design strategy. Semin. Oncol. 27,11 -19 (suppl).
Bungay, P.M., Dedrick, R.L., Fox, E., and Balis, F.M. (2001) Probe calibration in transient microdialysis in vivo. Pharm. Res. 18,361 -366.[CrossRef][ISI][Medline]
Cairncross, G., Swinnen, L., Bayer, R., Rosenfeld, S., Salzman, D., Paleolo gos, N., Kaminer, L., Forsyth, P., Stewart, D., Peterson, K., Hu, W., Mac donald, D., Ramsay, D., and Smith, A., for the Oligodendroglioma Study Group (2000) Myeloablative chemotherapy for recurrent aggressive oligodendroglioma. Neuro-Oncol. 2, 114-119.[Abstract]
Chabner, B.A., Boral, A.L., and Multani, P. (1998)
Translational research: Walking the bridge between idea and
cure—Seventeenth Bruce F. Cain Memorial Award Lecture. Cancer
Res. 58,4211
-4216.
DeAngelis, L.M. (2001) Brain tumors. N.
Engl. J. Med. 344,114
-123.
de Lang, E.C., de Vries, J.D., Zurcher, C., Danhof, M., de Boer, A.G., and Breimer, D.D. (1995a) The use of intracerebral microdialysis for the determination of pharmacokinetic profiles of anticancer drugs in tumor-bearing rat brain. Pharm. Res. 12,1924 -1931.[CrossRef][ISI][Medline]
de Lang, E.C., Danhof, M., Zurcher, C., de Boer, A.G., and Breimer, D.D. (1995b) Repeated microdialysis perfusions: Periprobe tissue reactions and BBB permeability. Brain Res. 702,261 -265.[CrossRef][ISI][Medline]
de Lang, E.C., Danhof, M., de Boer, A.G., and Breimer, D.D. (1997) Method ological considerations of intracerebral microdialysis in pharmacokinetic studies on drug transport across the blood-brain barrier. Brain Res. Rev. 25, 27-49.[CrossRef][Medline]
De Micheli, E., Alfieri, A., Pinna, G., Bianchi, L., Colivicchi, M.A., Melani, A., Pedata, F., Della Corte, L., and Bricolo, A. (2000) Extracellular levels of taurine in tumoral, peritumoral, and normal brain tissue in patients with malignant glioma: An intraoperative microdialysis study. Adv. Exp. Med. Biol. 483,621 -625.[ISI][Medline]
Devineni, D., Klein-Szanto, A., and Gallo, J.M.
(1996a) Uptake of temo zolomide in a rat glioma model in the
presence and absence of the angiogenesis inhibitor TNP-470. Cancer
Res. 56,1983
-1987.
Devineni, D., Klein-Szanto, A., and Gallo, J.M. (1996b) In vivo microdialysis to characterize drug transport in brain tumors: Analysis of methotrexate uptake in rat glioma-2 (RG-2)-bearing rats. Cancer Chemother. Pharmacol. 38,499 -507.[CrossRef][ISI][Medline]
Disabato, J.A., Handler, M.H., Strain, J.D., Fleitz, J.M., and Foreman, N.K. (1999) Successful use of intracavitary bleomycin for low-grade astrocy toma tumor cyst. Ped. Neurosurg. 31,246 -250.
Dropcho, E.J. (2001) Novel chemotherapeutic approaches to brain tumors. Hematol. Oncol. Clin. North Am. 15,1027 -1052.[CrossRef][ISI][Medline]
Dukic, S., Kaltenbach, M.L., Gourdier, B., Marty, H., and Vistelle, R. (1998) Determination of free extracellular levels of methotrexate by microdialysis in muscle and solid tumor of the rabbit. Pharm. Res. 15,133 -138.[CrossRef][ISI][Medline]
During, M.J., and Spencer, D.D. (1993) Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341,1607 -1610.[CrossRef][ISI][Medline]
Dykstra, K.H., Hsiao, J.K., Morrison, P.F., Bungay, P.M., Mefford, I.N., Scully, M.M., and Dedrick, R.L. (1992) Quantitative examination of tissue con centration profiles associated with microdialysis. J. Neurochem. 58,931 -940.[ISI][Medline]
Elmquist, W.F., and Sawchuk, R.J. (1997) Application of microdialysis in pharmacokinetic studies. Pharm. Res. 14,267 -288.[CrossRef][ISI][Medline]
Fox, E., Curt, G.A., and Balis, F.M. (2002a) Clinical
trial design for target-based therapy. Oncologist
7, 401-409.
Fox, E., Bungay, P.M., Bacher, J., McCully, C.L., Dedrick, R.L.,
and Balis, F.M. (2002b) Zidovudine concentration in brain
extracellular fluid measured by microdialysis: Steady-state and transient
results in rhesus monkey. J. Pharmacol. Exp. Ther.
301,1003
-1011.
Gibaldi, M., and Perrier, D. (1982)Pharmacokinetics, 2nd ed. New York: Marcel Dekker, Inc.
Gopinath, S.P., Valadka, A.B., Goodman, J.C., and Robertson, C.S. (2002) Extracellular glutamate and aspartate in head injured patients. Acta Neurochir. Suppl. 76,437 -438.
Graham, M.L., Herndon, J.E., 2nd, Casey, J.R., Chaffee, S., Ciocci,
G.H., Krischer, J.P., Kurtzberg, J., Laughlin, M.J., Longee, D.C., Olson,
J.F., Paleologus, N., Pennington, C.N., and Friedman, H.S. (1997)
High-dose chemotherapy with autologous stem-cell rescue in patients with
recurrent and high-risk pediatric brain tumors. J. Clin.
Oncol. 15,1814
-1823.
Groothuis, D.R., Ward, S., Schlageter, K.E., Itskovich, A.C., Schwerin, S.C., Allen, C.V., Dills, C., and Levy, R.M. (1998) Changes in blood-brain bar rier permeability associated with insertion of brain cannulas and microdialysis probes. Brain Res. 803,218 -230.[CrossRef][ISI][Medline]
Haines, S.J. (2002) Moving targets and ghosts of the past: Outcome mea surement in brain tumour therapy. J. Clin. Neurosci. 9,109 -112.[CrossRef][ISI][Medline]
Hargrave, D.R., Bouffet, E., Gammon, J., Tariq, N., Grant, R.M., and Baruchel, S. (2002) Phase I study of fotemustine in pediatric patients with refractory brain tumors. Cancer 95,1294 -1301.[CrossRef][ISI][Medline]
Haroun, R.I., Clatterbuck, R.E., Gibbons, M.C., Burger, P.C., Parker, R., Frue hauf, J.P., and Brem, H. (2002) Extreme drug resistance in primary brain tumors: In vitro analysis of 64 resection specimens. J. Neurooncol. 58,115 -123.[CrossRef][Medline]
Hlatky, R., Furuya, Y., Valadka, A.B., Goodman, J.C., and Robertson, C.S. (2002) Comparison of microdialysate arginine and glutamate levels in severely head-injured patient. Acta Neurochir. Suppl. 81,347 -349.[Medline]
Hutchinson, P.J., Gupta, A.K., Fryer, T.F., Al-Rawi, P.G., Chatfield, D.A., Coles, J.P., O'Connell, M.T., Kett-White, R., Minhas, P.S., Aigbirhio, F.I., Clark, J.C., Kirkpatrick, P.J., Menon, D.K., and Pickard, J.D. (2002) Correlation between cerebral blood flow, substrate delivery, and metabolism in head injury: A combined microdialysis and triple oxygen positron emission tomography study. J. Cereb. Blood Flow Metab. 22,735 -745.[ISI][Medline]
Kellie, S.J., Barbaric, D., Koopmans, P., Earl, J., Carr, D.J., and de Graaf, S.S. (2002) Cerebrospinal fluid concentrations of vincristine after bolus intravenous dosing: A surrogate marker of brain penetration. Cancer 94,1815 -1820.[CrossRef][ISI][Medline]
Kennedy, R.T., Watson, C.J., Haskins, W.E., Powell, D.H., and Strecker, R.E. (2002) In vivo neurochemical monitoring by microdialysis and capillary separations. Curr. Opin. Chem. Biol. 6,659 -665.[CrossRef][ISI][Medline]
Koopmans, P.P. (2002) Clinical endpoints in trials of
drugs for cancer: Time for a rethink? B.M.J.
324,1389
-1391.
Korppi-Tommola, T., Huhmar, H., Aronen, H.J., Penttila, P., Hiltunen, J., Savolainen, S., Kallio, M.E., and Liewendahl, K. (1999) 111In-labelled bleomycin complex for the differentiation of high- and low-grade gliomas. Nuclear Med. Commun. 20,145 -152.[ISI][Medline]
Kraemer, D.F., Fortin, D., and Neuwelt, E.A. (2002) Chemotherapeutic dose intensification for treatment of malignant brain tumors: Recent developments and future directions. Curr. Neurol. Neurosci. Rep. 2,216 -224.[Medline]
Lesniak, M.S., Langer, R., and Brem, H. (2001) Drug delivery to tumors of the central nervous system. Curr. Neurol. Neurosci. Rep. 1,210 -216.[Medline]
Lonnroth, P., Jansson, P.A., and Smith, U. (1987) A microdialysis method allowing characterization of intracellular water space in humans. Am. J. Physiol. 253,E228 -E231.
Lowe, E., and Balis, F.M. (2001) Dose-effect and concentration-effect analy sis. In: Atkinson, A.J., Jr., Daniels, C.E., Deddrick, R.L., Grudzinskas, C.V., and Markey, S.P. (Eds.), Principles of Clinical Phamacology, San Diego, Calif.: Academic Press. pp. 235-244.
Ma, J., Pulfer, S., Li, S., Chu, J., Reed, K., and Gallo, J.M.
(2001) Pharmacodynamic-mediated reduction of temozolomide tumor
concentrations by the angiogenesis inhibitor TNP-470. Cancer
Res. 61,5491
-5498.
Ma, J., Li, S., Reed, K., Guo, P., and Gallo, J.M.
(2003) Pharmacodynamic-mediated effects of the angiogenesis
inhibitor SU5416 on the tumor dis position of temozolomide (TMZ) in
subcutaneous and intracerebral human glioma xenograft models. J.
Pharmacol. Exp. Ther. 305,833
-839.
Marion, D.W., Puccio, A., Wisniewski, S.R., Kochanek, P., Dixon, C.E., Bul lian, L., and Carlier, P. (2002) Effect of hyperventilation on extracellular concentrations of glutamate, lactate, pyruvate, and local cerebral blood flow in patients with severe traumatic brain injury. Crit. Care Med. 30,2619 -2625.[CrossRef][ISI][Medline]
Meixensberger, J., Kunze, E., Barcsay, E., Vaeth, A., and Roosen, K. (2001) Clinical cerebral microdialysis: Brain metabolism and brain tissue oxy genation after acute brain injury. Neurol. Res. 23,801 -806.[CrossRef][ISI][Medline]
Meyerson, B.A., Linderoth, B., Karlsson, H., and Ungerstedt, U. (1990) Microdialysis in the human brain: Extracellular measurements in the thal amus of parkinsonian patients. Life Sci. 46,301 -308.[CrossRef][ISI][Medline]
Morgan, M.E., Singhal, D., and Anderson, B.D. (1996)
Quantitative assessment of blood-brain barrier damage during microdialysis.
J. Pharmacol. Exp. Ther.
277,1167
-1176.
Muller, M. (2000) Microdialysis in clinical drug delivery studies. Adv. Drug Deliv. Rev. 45,255 -269.[CrossRef][ISI][Medline]
Muller, M., Mader, R.M., Steiner, B., Steger, G.G., Jansen, B.,
Gnant, M., Hel bich, T., Jakesz, R., Eichler, H.G., and Blochl-Daum, B.
(1997) 5-Fluorouracil kinetics in the interstitial tumor space:
Clinical response in breast cancer patients. Cancer
Res. 57,2598
-2601.
Nilsson, O.G., Saveland, H., Boris-Moller, F., Brandt, L., and Wieloch, T. (1996) Increased levels of glutamate in patients with subarachnoid haemorrhage as measured by intracerebral microdialysis. Acta Neurochir. Suppl. (Wien) 67, 45-47.[Medline]
Oertel, M., Kelly D.F., Lee, J.H., McArthur, D.L., Glenn, T.C., Vespa, P., Boscardin, W.J., Hovda, D.A., and Martin, N.A. (2002) Efficacy of hyperventilation, blood pressure elevation, and metabolic suppression therapy in controlling intracranial pressure after head injury. J. Neurosurg. 97,1045 -1053.[ISI][Medline]
Persson, L., and Hillered, L. (1992) Chemical monitoring of neurosurgical inten sive care patients using intracerebral microdialysis. J. Neurosurg. 76, 72-80.[ISI][Medline]
Planas, A.M., Justicia, C., Sole, S., Friguls, B., Cervera, A., Adell, A., and Chamorro, A. (2002) Certain forms of matrix metalloproteinase-9 accumulate in the extracellular space after microdialysis probe implantation and middle cerebral artery occlusion/reperfusion. J. Cereb. Blood Flow Metab. 22,918 -925.[CrossRef][ISI][Medline]
Rall, D.P., and Zubrod, C.G. (2000) Mechanisms of drug absorption and excretion: Passage of drugs in and out of the central nervous system. In: Abeloff, M.D. (Ed.), Clinical Oncology, 2nd ed., New York: Churchill Livingstone, pp.109 -128.
Roche, H., Cure, H., Adenis, A., Fargeot, P., Terret, C., Lentz, M.A., Madelmont, J.C., Fumoleau, P., Hanausk, A., and Chollet, P. (2000) Phase II trial of cystemustine, a new nitrosourea, as treatment of high-grade brain tumors in adults. J. Neurooncol. 49,141 -145.[CrossRef][Medline]
Roslin, M., Henriksson, R., Bergström, P., Ungerstedt, U., and Bergenheim, T.A. (2003) Baseline levels of glucose metabolites, glutamate and glyc erol in malignant glioma assessed by stereotactic microdialysis. J. Neurooncol. 61,151 -160.[CrossRef][Medline]
Ryynanen, P.M., Savolainen, S.E., Aronen, H.J., Korppi-Tommola, E.T., Huh mar, H.M., Kallio, M.E., and Hiltunen, J.V. (1998) Kinetics of 111In-labeled bleomycin in patients with brain tumors: Compartmental vs. non-compartmental models. Ann. Nuclear Med. 12,313 -321.
Sun, H., Bungay, P.M., and Elmquist, W.F. (2001)
Effect of capillary efflux transport inhibition on the determination of probe
recovery during in vivo microdialysis in the brain. J. Pharmacol.
Exp. Ther. 297,991
-1000.
Tokunaga, Y., Nakashima, M., Sasaki, H., Tomiyama, N., Nakashima, M.N., Ichikawa, M., Kaminogo, M., and Shibata, S. (2000) Local distribution into brain tumor and pharmacokinetics of 4-pyridoxate diammine hydroxy platinum, a novel cisplatin derivative, after intracarotid admin istration in rats with 9L malignant glioma: Simultaneous brain microdial ysis study. Biol. Pharm. Bull. 23,1491 -1496.[ISI][Medline]
Ungerstedt, U., and Pycock, C. (1974) Functional correlates of dopamine neurotransmission. Bull. Schweizerischen Akad. Med. Wiss. 30,44 -55.
Vespa, P., Prins, M., Ronne-Engstrom, E., Caron, M., Shalmon, E., Hovda, D.A., Martin, N.A., and Becker, D.P. (1998) Increase in extracellular glutamate caused by reduced cerebral perfusion pressure and seizures after human traumatic brain injury: A microdialysis study. J. Neurosurg. 89,971 -982.[ISI][Medline]
Vespa, P.M., McArthur, D., O'Phelan, K., Glenn, T., Etchepare, M., Kelly, D., Bergsneider, M., Martin, N.A., and Hovda, D.A. (2003) Persistently low extracellular glucose correlates with poor outcome 6 months after human traumatic brain injury despite a lack of increased lactate: A microdialysis study. J. Cereb. Blood Flow Metab. 23,865 -877.[ISI][Medline]
Wang, Y., Wong, S.L., and Sawchuk, R.J. (1993) Microdialysis calibration using retrodialysis and zero-net flux: Application to a study of the distri bution of zidovudine to rabbit cerebrospinal fluid and thalamus. Pharm. Res. 10,1411 -1419.[CrossRef][ISI][Medline]
Winter, C.D., Iannotti, F., Pringle, A.K., Trikkas, C., Clough, G.F., and Church, M.K. (2002) A microdialysis method for the recovery of IL-1beta, IL-6 and nerve growth factor from human brain in vivo. J. Neurosci. Methods 119, 45-50.[CrossRef][ISI][Medline]
Zamboni, W.C., Gervais, A.C., Egorin, M.J., Schellens, J.H.,
Hamburger, D.R., Delauter, B.J., Grim, A., Zuhowski, E.G., Joseph, E., Pluim,
D., Pot ter, D.M., and Eiseman, J.L. (2002) Inter- and
intratumoral disposition of platinum in solid tumors after administration of
cisplatin. Clin. Cancer Res.
8,2992
-2999.
This article has been cited by other articles:
|
|
 |
|
  W. Yang, R. F. Barth, G. Wu, M. J. Ciesielski, R. A. Fenstermaker, B. A. Moffat, B. D. Ross, and C. J. Wikstrand Development of a Syngeneic Rat Brain Tumor Model Expressing EGFRvIII and Its Use for Molecular Targeting Studies with Monoclonal Antibody L8A4 Clin. Cancer Res., January 1, 2005; 11(1): 341 - 350. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. F. Barth, W. Yang, A. S. Al-Madhoun, J. Johnsamuel, Y. Byun, S. Chandra, D. R. Smith, W. Tjarks, and S. Eriksson Boron-Containing Nucleosides as Potential Delivery Agents for Neutron Capture Therapy of Brain Tumors Cancer Res., September 1, 2004; 64(17): 6287 - 6295. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
|
