Studies on the Uptake of Vitamin B12-Co60
by the Hamster
Methylcholanthrene-induced
Sarcoma and the Rat
Walker Carcinosarcoma*
A. MILLER,t G. GAULL,H. M. LEMON,ANDJ. F. RossJ
(Robert Dateson Erans Memorial, Massachusetts Memorial Hospitals, and Department
Boston University School of Medicine, Boston, Afa*«.)
Many studies (10, 12, 15) have demonstrated
the key role of vitamin Bi2 in normal growth and
development. Oleson (16) found that supplemen
tary vitamin B^ caused increased growth of the
Rous sarcoma in chicks. This observation suggest
ed that vitamin BK might be necessary for the
growth of malignant neoplasms. With the use of
isotopically labeled vitamin Bi2, the possible rela
tionship of vitamin B^ to tumor metabolism has
been investigated.
the heavier organs 30 ml. of 2 N NaOH was used. The tissues
were digested in alkali at room temperature for 24 hours. Then,
if necessary, gentle heating for 30-60 seconds brought the gellike digest into a liquid state. Measurements of radioactivity
were made on duplicate 4-rnl. aliquots of these tissue digests.
The total volume of the tissue digest solution was assumed to
be equal to 10 ml. when the organ weight was less than 0.75
gm., since the volume contributed by the dissolved organ was
negligible. For heavier organs the total volume of the digest
was measured in a 25- or 100-ml. graduated cylinder.
Urine and stools.—
In the rat the total urine volume was meas
ured in a 50-ml. graduated cylinder. Radioactivity was deter
mined on 4-ml. aliquots of urine. For hamsters the filter paper
on which the urine had dried was cut into }-inch pieces and
placed into If X 8¿-inchglass bottles in which radioactivity
was measured. The radioactivity in 4-day stool collections
was also measured in 1} X 3i-inch glass bottles.
Carcasses.—Therat carcasses were placed into i\ X 6-inch
glass bottles. Carcass radioactivity measurements were made
in these bottles.
MATERIALS AND METHODS
EXPERIMENTAL
PLAN
Adult male hamsters weighing from 75 to 100 gm., bearing
a methylcholanthrene-induced sarcoma as previously de
scribed (8, 11), and adult male Sprague-Dawley rats weighing
from 220 to 880 gm., bearing the Walker carcinosarcoma, were
used in these studies. These animals were housed in individual
cages, at constant temperature, and fed stock diet and water
ad libitum. Under light ether anesthesia, they were given sub
cutaneous injections of vitamin Biz-Co60(secured from Merck
& Co., Rahway, N.J.), receiving 0.10-0.50 pg. of vitamin Bi2,
equivalent to 0.09-0.40 /ic. of Co60,contained in a total volume
of 1.0 ml. After the injection, rats were housed in metabolic
cages allowing for separate urine and stool collections. The
hamsters were housed in wire cages, under which were placed
pans which were covered with two thicknesses of Whatman
filter paper #8. All stools fell on the paper while the urine was
absorbed into the paper. Animals were sacrificed 4 days follow
ing the injection of vitamin Bi2-Co60except in the turnover and
flushing experiments, in which the animals were killed at the
times indicated in the text.
PREPARATIONOFSPECIMENSFORANALYSIS
Organs.—Theliver, kidneys, spleen, heart, and tumor were
removed and weighed. Organs weighing less than 5.0 gm. were
placed into flasks containing 10 ml. of 2 N NaOH, whereas with
* This work was supported in part by grants from the Unit
ed States Public Health Service and The Atomic Energy
Commission.
t Formerly U.S. Public Health Service Fellow. Present
address: Boston Veterans Administration Hospital, Boston,
Mass.
ÃŽ
Present address: University of California Medical Center,
Los Angeles, Calif.
Received for publication March 12, 1956.
of Medicine,
RADIOACTIVITY
DETERMINATION
A 1:100 dilution of the injected vitamin Bi2-Co'°
was made,
and varying aliquots were then used as standards for the vary
ing conditions employed in the counting of organ digests,
excreta, and carcasses. By the addition of water as needed, the
height of the standard in the glass bottles was always the same
as that of the specimen being counted, i.e., stools, urine, or
carcasses. Organ and liquid urine samples were counted in a
scintillation well-type counter (thallium-activated, sodium
iodide, scintillation crystal). The radioactivity count of the
organ samples usually was 3-12 X background count, except
for the heart and spleen, for which the counts were usually
1-3 X background. Samples were counted long enough to give
a counting error of less than 2 per cent, except for the lowcount samples, for which a 5-8 per cent counting accuracy was
obtained. Duplicate samples usually agreed within 1-5 per
cent. The radioactivity of all samples contained in the li X
8J-inch glass bottles was determined by placing them on top of
the above-mentioned sodium iodide well crystal. The diameter
of these bottles was just equal to that of the diameter of the
well. Under similar geometric conditions, the radioactivity of a
standard was also determined. The 6-inch bottles containing
the rat carcasses were marked into three equal 2-inch segments.
With the bottle in the horizontal position and directly in con
tact with a solid 1 X 1-inch thallium-activated, sodium iodide
crystal, the radioactivity of each 2-inch segment of the bottle
containing the carcass was counted. Under similar geometric
conditions, the radioactivity of the bottle containing the stand
ard was measured.
842
Downloaded from cancerres.aacrjournals.org on June 14, 2017. © 1956 American Association for Cancer Research.
MILLERet al.—Radioactive Vitamin BU in Animal Tumors
843
ranged from 11.4 to 29.6 per cent at both dosage
levels. Furthermore, the tumor was the major
site of vitamin B12-Co60localization with these
counts/min/ml organ digest X total volume digest
X 100;
implants in the back, which grow to much larger
counts/min injected
sizes than the cheek pouch implants.
The radioactivity uptake of the rat Walker carcinototal counts/min in organ
counts/min/gm organ
weight of organ (gm)
sarcoma.—Eight rats with Walker carcinosarcomas weighing from 5.1 to 82.7 gm. took up from
RESULTS
1.5 to 16.2 per cent of the injected radiovitamin
The radioactivity uptake of the hamster methyl(Table 3). In four of the eight rats, the tumor was
cholanthrene-induced sarcoma.—Hamster methylthe organ with the greatest content of radioac
cholanthrene-induced sarcomas, implanted in the
tivity. Except for a decreased kidney uptake, the
cheek pouch, weighing from 0.25 to 1.00 gm., took distribution of radioactivity in the other organs
up 1.2-3.1 per cent of the injected radioactivity
was similar to that found for normal rats. When
the total uptake was related to organ weight, the
TABLE 1
tumor uptake was approximately one-sixteenth
THE TISSUEDISTRIBUTION
OFRADIOACTIVITY
FOLLOW that of the kidneys and approximately one-half
INGTHEPARENTERAL
ADMINISTRATION*
OFVITAMIN
that of the liver, spleen, and heart (Table 3).
Bi2-CoM
TOHAMSTERS
BEARING
THEMETHYLCHOLANCALCULATIONS
The per cent radioactivity in organ =
THHENE-INDUCED
CHEEK POUCH SARCOMA
TABLE 2
ofinjectedradioactivityin
cent
COMPARISON
BETWEEN
Two GROUPS
OFHAMSTERS
IN
JECTEDWITHDOTERENT
DOSESOFVITAMINBn-Co60
organ6.46.66.416.911.819.411.71.21.31.53.10.30.30.30.30.20.10.40.4
OrganKidneyLiverSarcomaHeartSpleenHamsterno.1S412S41234i2341234Wt.(gm.)0.4900.6400.6421.8402.1682.4842.4730.2510.3350.4291.0000.2400.2550.2600.2330.0320.0200.1100
ASTOSARCOMA
UPTAKEOFRADIOACTIVITY
Per cent of
Group I*
Mean
Group Hf
Animal
1
2
3
Weight of
larcoma
(gm.)
injected
radioactivity
in sarcoma
16.35
7.20
31.70
26.5
12.6
29.5
1301
1178
771
18.42
33.96
21.00
5.97
22.8
25.2
22.8
11.4
1083
2513
6487
6145
Mean
20.30
19.8
* Dose = 0.09 /ic. = 0.10 /ig. of vitamin BH.
t Dose = 0.36 ite. = 0.40 ¿igof vitamin B1S.
Counts/rain/
gm
5048
Relationship of the size of the tumor to vitamin
Bi2-Cow uptake.—Chart 1 demonstrates the corre
lation between tumor size and the per cent uptake
(Table 1). The distribution of radioactivity in the of vitamin Bi2-Co80by the hamster sarcoma both
liver, kidney, and other viscera was similar to that in the cheek pouch and on the back. There was a
found in normal hamsters. When the total uptake
good correlation between the uptake of radioac
was related to organ weight, the tumor uptake was tivity and the tumor size for tumors weighing less
approximately ^ that of the kidney, | that of the than 17.5 gm. With the heavier tumors the in
liver, similar to that of the spleen, and 3 times that crease in vitamin Bu-Co60 uptake was not com
mensurate with increases in their weight. The rat
of the heart (Table 1).
Effect of size of dose on the uptake of radioactivity Walker carcinosarcoma showed a similar relation
in hamster methylcholanthrene-induced sarcoma.— ship between tumor radioactivity uptake and size.
Two groups of hamsters with large methylcholan
Thus, with Walker carcinosarcomas weighing less
threne-induced sarcomas implanted in the back than 40.3 gm., a fair correlation was found be
tween vitamin Bw-Co60uptake and size. However,
were given injections of 0.1 and 0.4 ¿tg.
of vitamin
Biz-Co60.No major difference in the sarcoma con
with the heavier tumors, this relationship no long
tent of radioactivity (expressed as per cent of ad
er obtained (Table 3).
ministered dose) was found at these two dosage
The turnover of radioactivity in the hamster sarco
ma.—The turnover of radioactivity in the tumors
levels (Table 2). The tumor uptake of radioactivity
* Dose—0.45MC.Co«= 0.50 /ig. Vitamin B12.
Downloaded from cancerres.aacrjournals.org on June 14, 2017. © 1956 American Association for Cancer Research.
844
Cancer Research
and organs of hamsters sacrificed at varying inter
vals up to 45 days was studied. The per cent radio
activity in the sarcoma over a 45-day period was
relatively constant, i.e., there was a negligible rate
of turnover (Chart 2). The 9.7-19.5 per cent range
in the sarcoma content of radioactivity found dur
ing the 45 days was probably secondary to the dif
ference in the weights of the tumors (3.37-99.20
gm.) and to the varying degrees of necrosis found.
The per cent radioactivity
in the liver, kidney,
spleen, and heart also remained relatively con
stant. After the first 4 days urinary excretion of
radioactivity
was no longer present, whereas the
daily excretion of radioactivity
in the stools, al
though very small, continued over the whole 45day period.
"Flushing" experiment in rats bearing Walker
carcinosarcomas.—Two groups of rats bearing
Walker carcinosarcomas
were given injections of
vitamin Biz-Co60. Beginning \\ days after injec-
TABLE 3
THETISSUEDISTRIBUTION
OFRADIOACTIVITY
FOLLOWING
THEPARENTERAL
ADMINISTRATION*
OFVITAMIN
B,2-CoM
TORATSBEARING
THEWALKER
CARCINOSARCOMA
Per cent of injected
activity(couDti/min/gm)6,9834,65312,4603,1393,1396,2934,5262,6906498
radioactivity
Wt.(gm.)1.772.602.452.801.8»2.652.502.352.38
Liver
in organ
Rat no.
Organ
Kidney
1
2
3
4
6
6
7
8
Mean and S.E. of mean
1
2
8
4
5
6
7
8
8.6
8.4
21.9
6.1
8.7
•¿
.0
4.9
5.0
0.1314.4015.5115.2317.8119.4318.4223.4122.8318.S8±1.2034.709.405
+
±11341,0337784M6436297861,097771780
9.1±2.0
10.3
8.4
5.4
7.9
8.9
10.9
18.7
12.8
10.4 + 1 4
±71301426427305350551258301
Mean and S.E. of mean
Walker carcinosarcoma
1
2
9
4
5
6
7.3
2.8
1.5
1143
5163.4037
9.2
16 2
15 6
15.6
15.2
5382.7169.20Specific
7
8
Spleen
Heart
Mean and S.E. of mean
1
2
3
4
5
6
7
8
Mean and S.E. of mean
1
2
3
4
.5
6
7
8
43.20 + 9.78
78
32
70
08
86
1.46
1.52
1.48
1.7 ±0.21
1.04
1.28
1.02
1.02
Mean and S.E. of Mean
1.09 ±0.07
' Dose = 0.25 ite. Coâ„¢= 0.30 pg. vitamin BU.
365 ±34
861
758
538
608
1,219
771
788
1,214
10.4±1.7
845 ±87
404
703
896
637
1.0±0.1
0.3
0.7
06
0.5
660 ±102
0.5±0.1
10
06
0.6
18
1.2
0.8
09
1.4
Downloaded from cancerres.aacrjournals.org on June 14, 2017. © 1956 American Association for Cancer Research.
MILLERet al.—Radioactive Vitamin Bn in Animal Tumors
tion, one group of rats was given five daily "flush
ing" doses of nonradioactive vitamin BU. A
marked decrease in radioactivity was found in the
liver, carcass, and Walker carcinosarcoma of the
flushed animals as compared with the control
group (Chart 3). Slight differences in tumor size
between the two groups were present, but these
845
nary excretion of radioactivity rose to a mean of
11.0 per cent in the flushed group as compared
with a mean of 1.8 per cent in the nonflushed
group (Chart 3).
DISCUSSION
The hamster sarcoma and the Walker carcino
sarcoma concentrated appreciable amounts of the
injected vitamin Bi2-Co60.The uptake correlated
fairly well with the weight of the tumor. This rela
tionship was true for all but the heaviest tumors,
in which increases in tumor weight were associated
with only minimal increases in the uptake of vita
min Bi2-Co60. The necrosis found in the larger
tumors probably explains this finding.
10 - . •¿
RADIOACTIVITY
e5
IO
15
20
25
30
35
40
WEIGHT OF SARCOMA (CM.)
CHART1.—Correlation between the size of the inethylcholanthrerie-induccd sarcoma and the tumor uptake of vita
min Bi2-CoM.
»CAM
*AOlO*Crmrr
—¿
>nKIDNEY
cttlmnvat— 12912.9
mURINE
;02t44
.nCARCASS
itiLIVER
m TUMOR
16.UZ.5 11.4:1.2 160112
CHART3.—Changes in the tissue distribution and excretion
of a parenteral dose of vitamin Bij-CoMfollowing large flushing
doses of nonradioactive vitamin BU in rats bearing the Walker
carcinosarcoma.
* Refers to number of animals in each group.
** Flushed group received five daily SO-ftg. injections of
vitamin Hi- beginning I Õdays after the injection of 0.3 p%.of
vitamin B|2-Co60.
5
IO
DAYS AFTER
15
20
25
S.C. INJECTION
30
OF Co"
35
40
45
Vitamin 3g
CHART2.—Theturnover of tumor and organ radioactivity
after the parenteral administration of vitamin Bu-Co80 to
hamsters bearing the methylcholanthrene-induced sarcoma.
At each indicated time, the tumor and organ radioactivity
(per cent of injected dose) of two hamsters are given, except at
45 days, when only one hamster was used. The tumor and
organ turnover curves shown above were drawn through the
mean of each of the two given values. The weights of the ham
ster sarcomas at each indicated time are also shown.
differences were probably not large enough to ac
count for the results noted. In contrast, the kid
neys of the flushed animals contained only about
one-half the radioactivity of the kidneys of the
control animals.
Urinary excretion during the first 1| days (be
fore flushing) was identical for both groups (an
average of 5.7 per cent). Following flushing, uri-
In this study it would have been desirable to
administer a dose of vitamin Bj2 that did not ap
preciably alter the blood concentration of vitamin
BIZ, i.e., a "tracer" dose. The smallest doses of
vitamin Bu-Co60 compatible with accurate count
ing were thus employed. However, these doses
still exceeded the total blood vitamin Bw of the rat
(3) by about 10-11 times. The organ and tumor
uptake of the radiovitamin at such pharmacologi
cal dosage levels may not represent their uptake
of endogenous vitamin B^. Because of the size of
dose and the necrosis in the larger tumors, com
parison of the organ and tumor uptake of vitamin
Bi2-Co«°
is difficult.
In some of the larger hamster and rat neo
plasms, the tumor uptake of B^-Co60 was greater
than that of any other organ. It is possible that
depletion of vitamin Bi2 stores, with or without
evidence of tissue depletion of this vitamin, may
Downloaded from cancerres.aacrjournals.org on June 14, 2017. © 1956 American Association for Cancer Research.
846
Cancer Research
occur in such animals. In the human, widespread
carcinomatosis has not been associated with the
usual evidence of vitamin BIZ deficiency. The
peripheral neuropathy reported with some cases
of bronchogenic carcinoma (6, 9, 18) does not ap
pear to be due to a deficiency of vitamin Bi2.
The flushing experiment was conducted to de
termine to what extent the radiovitamin was
bound or altered 36 hours after injection. Since
large injections of vitamin Bi2 are largely excreted
in the urine (2, 14, 19), the appearance of radio
activity in the urine following such an injection
indicates exchange between the previously admin
istered radiovitamin and the nonradioactive
parenteral dose. The increase in kidney concentra
tion of radioactivity found in the "flushed" ani
mals is undoubtedly a reflection of this excretion,
further evidenced by the increase in urinary radio
activity. This increase in urinary radioactivity was
accompanied by a reduction in the radioactivity
in the liver, Walker carcinosarcoma, and carcass
of the "flushed" animals to about hah' that of the
control animals. This would indicate that at least
hah" of the administered radiovitamin was not
firmly bound or materially altered 36 hours after
injection, since exchange between the parenterally
administered vitamin and some radioactive inter
mediate seems unlikely. Approximately one-half
of the radioactivity in the carcass, liver, and Walk
er carcinosarcoma was not exchangeable, indicat
ing either firm "binding" or chemical alteration of
this portion of the injected radiovitamin. It is of
interest that the radiovitamin taken up by the
Walker carcinosarcoma was exchangeable, which
observation suggested that this tumor is not an
absolute metabolic "trap" for vitamin Bi2 analo
gous to that suggested for amino acids and pro
teins (4, 13). The results of this "flushing" experi
ment differ from those of Harte et al. (5) in a simi
lar study on normal rats.
Radioactivity as measured in this study merely
determines the presence of the Co60moiety of the
vitamin B^ molecule. Thus, the radioactivity may
be due to vitamin B^ and/or to an intermediate
degradation product of the vitamin. Barbee and
Johnson found the radioactivity in the rat kidney
to be due to vitamin B12 (1). Furthermore, after
parenteral administration of vitamin BIJ, intact vi
tamin Bi2 is excreted in the urine (7, 17). Thus, it
appears likely that the radioactivity found in the
kidneys in this study is due to vitamin B12.How
ever, insofar as the tumor and the other organs
are concerned this question cannot be answered.
The turnover of radioactivity in the hamster
sarcoma, liver, kidney, and spleen was negligible
over a 45-day period. A slow rate of turnover of
radioactivity in normal rat liver, kidney, and
spleen has also been described by Harte (5). As
tissue radioactivity measurements do not neces
sarily measure the intact radiovitamin molecule,
these findings do not necessarily reflect the true
metabolic turnover of vitamin Bi2-Co60in these
tissues.
The uptake of Bi2-Co60by tumor tissue suggests
that this vitamin may be important for the growth
of malignant tumors as well as for normal tissues.
Further studies should help in clarifying the role
of vitamin Bw in the metabolism of malignant
tumors.
SUMMARY AND CONCLUSIONS
1. The uptake of parenterally administered
vitamin B^-Co60 by the hamster methylcholanthrene-induced sarcoma and the rat Walker car
cinosarcoma was studied.
2. Vitamin Bu-Co60 was taken up by both the
hamster sarcoma and the Walker carcinosarcoma.
The uptake of vitamin Bi2-Co60correlated well
with tumor weight except for the heavier tumors.
3. Large tumors were the major sites of vita
min Bis-Co60localization in some animals.
4. The turnover of radioactivity in the methylcholanthrene-induced sarcoma of the hamster, as
well as in the kidneys, liver, and spleen, was neg
ligible.
5. Large doses of nonradioactive vitamin BU
administered If days after the injection of vitamin
Biz-Co80were associated with: (a) a decrease in
liver, carcass, and Walker carcinosarcoma radio
activity; (6) an increase in kidney radioactivity;
and (c) an increase in urinary excretion of radio
activity.
ACKNOWLEDGMENTS
The authors wish to acknowledge the valuable technical
assistance of Mrs. Mary Lou Turner.
REFERENCES
1. BARBEE,K. W., and JOHNSON,B. C. Metabolism of Radio
active Vitamin B]2 by the Rat. Proc. Soc. Exper. Biol. &
Med., 76:720-21, 1951.
2. CONLEY,C. L.; KREVANS,J. R.; CHOW,B. F.; BARROWS,
C.; and LANG, C. A. Observations on the Absorption,
Utilization and Excretion of Vitamin B«.J. Lab. & Clin.
Med., 38:84-94, 1951.
3. COUCH,J. R.; OLCESE,O.; WITTEN,P. W.; and COLBY,
R. W. Vitamin Bi2 Content of Blood from Various Species.
Am. J. Physiol., 163:77-80, 1950.
4. FENNINOER,L. D., and MIDER,G. B. Energy and Nitrogen
Metabolism in Cancer. Adv. Cancer Research, 2:229-53,
1954.
5. HARTE,R. A.; CHOW,B. F.; and BARROWS,
L. Storage and
Elimination of Vitamin Bu in the Rat. J. Nutrition, 49:
669-78, 1953.
Downloaded from cancerres.aacrjournals.org on June 14, 2017. © 1956 American Association for Cancer Research.
MILLERet al.—Radioactive Vitamin BÌ2
in Animal Tumors
6. HENSON,R. A.; RÃœSSEL,
D. S.; and WILKINSON,M. Carcinomatous Neuropathy and Myopathy. A Clinical and
Pathological Study. Brain, 77:82-121, 1954.
7. LANG,C.; HARTE,R. A.; CONLEY,C. L.; and CHOW,B. F.
Retention of Crystalline Vitamin Bi2 by Healthy Male
Individuals Following Intramuscular Injection. J. Nutri
tion, 46:215-21, 1952.
8. LEMON,H. M., and SMAKULA,
E. Factors Affecting Ham
ster Sarcoma Growth in the Cheek Pouch. Cancer Re
search, 16:273-79, 1955.
9. LENNOX,B., and PBICHARD,S. The Association of Bron
chial Carcinoma and Peripheral Neuritis. Quart. J. Med.,
19:97-109, 1950.
10. LUECKE,R. W.; McMiLLEN, W. M.; THORP,F., JR.; and
BONIECE,J. R. The Effects of Vitamin Bu Concentrate on
the Growth of Weanling Pigs Fed Corn Soy-Bean Diets.
Science, 110:139-40, 1949.
11. LUTZ,B. R.; FULTON,G. P.; PATT,D. I.; HANDLER,A. H.;
and STEVENS,D. F. The Cheek Pouch of the Hamster as
a Site for the Transplantation of a Methylcholanthreneinduced Sarcoma. Cancer Research, 11:64-66, 1951.
12. McCoLLUM, E. B., and CHOW,B. F. Sex Differences in
Weight-Stimulating Effects of Bis in Rats on Diets of
Varying Composition. Proc. Soc. Exper. Biol. & Med.,
76:20-28, 1950.
847
13. MIDER, G. B.; TESLTTK,
H.; and MORTON,J. J. Effects of
Walker Carcinoma 256 on Food Intake, Body Weight and
Nitrogen Metabolism of Growing Rats. Acta Union Inter
nat. Contre Cancer, 6:409-20, 1948.
14. MOLLIN,D. L., and Ross, G. I. M. Vitamin Bi2Concentra
tions of Serum and Urine in the First 72 Hours after Intra
muscular Injections of the Vitamin. J. Clin. Path., 6:54—
61, 1953.
15. NICHOL,C. A; DIETRICH,L. S.; CRAVENS,W. W.; and
ELVEHJEM,C. A. Activity of Vitamin Bi2 in the Growth of
Chicks. Proc. Soc. Exper. Biol. & Med., 70:40-42, 1949.
16. OLESON,J. J., and LITTLE,P. A. The Effect of Pteroylglutamic Acid and Vitamin Bi2 on Growth of Rous Sarcoma
Implants. Proc. Soc. Exper. Biol. & Med., 71:226-27,
1949.
17. ROSENBLUM,
C.; CHOW,B. F.; CONDON,G. P.; and YAMAMOTO, R. Oral Versus Parenteral Administration of
CoM-Labeled Vitamin B«to Rats. J. Biol. Chem., 198:91528, 1952.
18. SMITH, T. W., and WHITFIELD,A. G. W. Malignant
Sensory Neuropathy. Lancet, 2:282-85, 1955.
19. YAMAMOTO,
R.; BARROWS,
C. H.; LANG,C. A.; and CHOW,
B. F. Further Studies on the Absorption of Vitamin BU
Following Oral and Parenteral Administration. J. Nutri
tion, 45:507-19, 1951.
Downloaded from cancerres.aacrjournals.org on June 14, 2017. © 1956 American Association for Cancer Research.
Studies on the Uptake of Vitamin B12-Co60 by the Hamster
Methylcholanthrene-induced Sarcoma and the Rat Walker
Carcinosarcoma
A. Miller, G. Gaull, H. M. Lemon, et al.
Cancer Res 1956;16:842-847.
Updated version
E-mail alerts
Reprints and
Subscriptions
Permissions
Access the most recent version of this article at:
http://cancerres.aacrjournals.org/content/16/9/842
Sign up to receive free email-alerts related to this article or journal.
To order reprints of this article or to subscribe to the journal, contact the AACR Publications
Department at [email protected].
To request permission to re-use all or part of this article, contact the AACR Publications
Department at [email protected].
Downloaded from cancerres.aacrjournals.org on June 14, 2017. © 1956 American Association for Cancer Research.