[CANCER RESEARCH 48, 6313-6316, November 15, 1988]
Boron Neutron Capture Therapy of a Murine Melanoma1
Jeffrey A. Coderre,2 John A. Kalef-Ezra, Ralph G. Fairchild, Peggy L. Micca, Lawrence E. Reinstein,
and John D. Glass
Medical Department, Brookhaven National Laboratory, Upton, New York 11973 fJ. A. C, J. A. K-E., K. G. F., P. L. M., J. D. G.J; Department of Physiology and
Biophysics, Ml. Sinai School of Medicine, New York, New York 10029 fJ. D. G.J; Department of Radiation Oncology, State University of New York, Stony Brook,
New York 11794 fL. E. R.J; and University ofloannina. Medical School, Medical Physics Laboratory, loannina, Greece [J. A. K-E.]
ABSTRACT
Boron neutron capture therapy has been carried out on BALB/c mice
carrying the Harding-Passey melanoma s.c. on the thigh. /7-Boronophen-
ylalanine (BPA), a boronated analogue of natural melanin precursors,
was used to target boron selectively to melanoma. BPA was administered
to the mice either via i.p. injection or p.o. by intubation. '"It concentrations
in tumor ranged from 15 to 40 ppm depending on the route and timing of
administration. Irradiations with a predominantly thermal neutron beam
were performed at the Brookhaven Medical Research Reactor. In the
absence of BPA, only transient tumor growth delays were observed at
low neutron fluences. At 5 x Id'" n/m2, 4 of 22 tumors irradiated in the
absence of BPA underwent long-term tumor growth control; after p.o.
administration of BPA (40 ppm '"H in the tumor), the fraction of tumors
controlled increased to 11 of 19. The average dose to the tumor in the
latter group was 17.8 Gy, of which 14.8 Gy were due to the '"15neutron
capture reaction. The biological effectiveness of the absorbed dose from
the neutron capture reaction, at the 50% tumor control level, was found
to be twice that of 100 kVp X-rays.
INTRODUCTION
The major dose-limiting factor in cancer radiation therapy is
the tolerance level of normal tissues within or close to the
radiation field. In BNCT,3 thermal neutrons interact with boron
via the '°B(n,a)7Li reaction (1) to produce short-range (<10
firn), densely ionizing heavy charged particles which have a
large relative biological effectiveness (2-7). In principal, selec
tive localization of 10Bwithin the tumor should allow most of
the dose to be restricted to the tumor (7, 8). However, initial
clinical trials of BNCT for the treatment of glioblastoma mul
tiforme carried out between 1953 and 1961 at Brookhaven
National Laboratory and the Massachusetts General Hospital
were disappointing (9-11). Poor results were attributed to two
major factors: (a) the use of boron-containing compounds
which showed no selective accumulation in tumor; and (¿>) the
rapid attenuation in tissue of the incident thermal neutron
beam. The high thermal neutron fluence used resulted in exces
sive surface tissue exposure; viable tumor was found at depth
following the neutron irradiations. The substantial levels of
boron in blood during irradiation contributed to the damage to
normal brain vasculature (tumorrblood ratio, <1).
The development of boron-containing compounds with the
ability to concentrate in tumor tissue has renewed interest in
BNCT. Clinical trials of BNCT with the sulfhydryl boronohy-
dride Na2Bi2HuSH have been under way since 1968 in Japan
under the direction of Professor H. Hatanaka. Median post
operative survival is claimed to be longer than postoperative
survival of comparable patients treated with conventional ra-
Received 12/14/87; revised 7/12/88; accepted 8/15/88.
The costs of publication of this article were defrayed in part by the payment
of page charges. This article must therefore be hereby marked advertisement in
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1This work was supported in part by Grants CA42446 (J. A. C.) and DK10080
(J. D. G.) form the NIH and by Contract DE-AC02-76CH00016 with the United
States Department of Energy. Accordingly the United States Government retains
a nonexclusive, royalty-free license to publish or reproduce the published form of
this contribution or allow others to do so for United States Government purposes.
2To whom requests for reprints should be addressed.
3 The abbreviations used are: BNCT, boron neutron capture therapy; BPA, p-
boronophenylalanine; BMRR, Brookhaven Medical Research Reactor.
diotherapy. Some long-term survivals (>8 years) have been
reported after operation and BNCT of malignant brain tumors
(12).
Further improvements are expected in BNCT from the use
of epithermal neutron beams to improve tissue penetration (13,
14). The potential of BNCT should be realized when epithermal
neutron beams can be combined with boron-containing com
pounds that concentrate in tumor with low boron levels in
blood and surrounding normal tissues. A number of laboratories
in the United States, Europe, Japan, and Australia are engaged
in the development of such compounds. We have recently
shown that a boron-containing amino acid analogue, BPA (15),
is transiently concentrated in a murine melanoma model with
optimal conditions for tumor treatment occurring about 6h
after injection (16). Within the tumor, BPA accumulation was
greatest in areas identified by trinateti thymidine autoradiog-
raphy as rapidly dividing tumor tissue and peaked 6 h after a
single i.p. injection. Tumor to nontumor boron concentration
ratios were 3:1 to 15:1. The amount of 10B in tumor ranged
from 15 to 30 ppm which is estimated to be adequate for BNCT
in vivo ( 13).
We have found that p.o. delivery of BPA results in signifi
cantly higher amounts of 10B in tumor than we were able to
obtain via i.p. injections. We now report the results of BNCT
experiments carried out at the BMRR using a murine mela
noma and the biochemically targeted boron carrier BPA.
MATERIALS AND METHODS
Murine Melanoma. Adult female BALB/c mice ( 15-20 g, 8-16 weeks
old) in which the Harding-Passey melanoma had been implanted s.c.
on the thigh were used. This tumor has been maintained in our
laboratory by serial transplantation for over 10 years and is reproducible
with respect to melanin content and uptake of melanin-affinic agents.
Melanin content (0.68% melanin by weight) is analogous to that found
in human melanotic melanoma (0.1-0.8%; average value, 0.35%) (17).
The Harding-Passey melanoma grows at the original s.c. implantation
site and does not metastasize. The s.c. location of this heavily pigmented
tumor facilitates volume measurements. Tumors weighing between 20
and 80 mg were chosen for therapy experiments. The initial tumor
dimensions ranged from 2.5 to 6 mm with an average thickness of
about 2 mm. This corresponds to 14-18 days of growth. Tumors that
have grown to this size do not undergo spontaneous remission. Mice
with untreated tumors or mice with tumors which eventually resumed
growth following the irradiation procedures were sacrificed when the
tumors exceeded 2-3 cm3. Mice whose tumors did not regrow after
therapy were monitored until they neared the end of their normal life-
span (an additional 18 months).
To test our presumption that thermal neutron irradiation in the
presence of BPA increases the radiosensitivity of the Harding-Passey
melanoma, tumor-bearing mice were divided into four groups: (a)
untreated controls; (b) irradiated with conventional X-rays; (c) irradi
ated at the BMRR in the absence of BPA; and (¡I)irradiated at the
BMRR following administration of BPA. A total of 187 tumor-bearing
mice were used; 40 mice served as untreated controls to document the
normal growth rate of this tumor, 56 to determine the sensitivity of the
Harding-Passey melanoma to conventional X-rays, 39 to determine the
response of the melanoma to neutron irradiation at the BMRR, and 52
to determine the response to irradiation in the presence of BPA.
6313
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