Hemoglobin Level and Tumor Growth*
Alfred Taylor, Ph.D., and Maxwell A. Pollack, Ph.D.
(From the Biochemical Institttte, University o/ Texas, Austin, Texas)
(Received for publication November 28, I94I)
T h e association of a n e m i a w i t h cancer has b e e n
reported for m a n y d i f f e r e n t types of a n i m a l s . It has
been r e p e a t e d l y o b s e r v e d t h a t t h e later stages of m a l i g r a n t g r o w t h s are c h a r a c t e r i z e d by a severe a n d progressive depression in the b l o o d h e m o g l o b i n level. T h i s
has b e e n f o u n d to be t r u e of m a n y d i f f e r e n t types a n d
[ocations of cancer in m a n , mice, rats, rabbits, birds,
:tc. (I, 2, 4, 5, 9, I3, I5)I n r e p o r t i n g t h e i r observations of this effect m o s t
w o r k e r s have described it as a " s e c o n d a r y a n e m i a " a n d
in g e n e r a l consider it to be t h e result of t h e g e n e r a l
Loxic action of the cancer o n t h e host. S u c h c o n d i t i o n s
as h e m o r r h a g e , infection, t h e presence of necrotic
tissue, a n d g e n e r a l d e b i l i t a t i o n have b e e n s u g g e s t e d as
m e d i a t i n g factors (I, 3, I4)"
T h e possibility t h a t c a n c e r o u s g r o w t h s m a y h a v e a
direct a n d d e s t r u c t i v e effect o n h e m o g l o b i n or i n h i b i t
its p r o d u c t i o n has n o t a p p a r e n t l y b e e n seriously considered.
It has been recently shown by Craig et al. (8) that the concentration of cytochrome C in cancer tissue is lower than in normal tissue. Greenstcin and co-workers (io) also recently reported that the introduction of liver tumor tissue into an animal
produced a very rapid and striking decrease in the liver catalase concentration. Both of these observations indicate that
cancer tissue has an antagonistic action on enzyme systems of
this type and since both cytochrome and catalase enzymes have
the same type of hemin prosthetic groups as hemoglobin, it
would not be surprising to find that hemoglobin was acted
upon in the same manner by tumorous tissue. These considerations could conceivably account for the striking anemia characteristic of the later stages of cancer, which is referred to above.
However, in the advanced period it is difficult to dissociate the
primary from the secondary effects of tumor growth. For that
reason the problem necessitates the study of the precancerous
and early cancerous conditions. Under these circumstances, significant decreases in the blood hemoglobin concentration should
constitute fairly valid indications of an antagonism between
cancer tissue and hemoglobin.
Strong has painted a clear picture of the blood hemoglobin
in relation to inherited cancer susceptibility and resistance in
mice. In a series of investigations (i6-i9) he has shown that
the hemoglobin level of mice of high spontaneous tumor incidence falls off markedly long before cancerous growths appear,
in contrast to cancer-resistant strains which do not react in this
manner. However, he considers this genetically-determined
effect to be unrelated to the anemia which appears after cancer
develops and which he speaks of as being secondary in nature.
So far as can be ascertained, no one has investigated the effect
This investigation was gcnerously supported by the Clayton
Foundation, Houston, Texas.
of a chemically-induced precancerous stage on the hemoglobin
level.
In studies which utilized several varieties of rabbits, Casey,
Pearce, and co-workers reported (6, 7, I~) that the resistance
of these animals to implanted malignant tmnors was related
to the hemoglobin level which prevailed before tumor inoculation. They found that the most resistant animals were those
with "normal" blood hemoglobin concentrations and red blood
cell counts while rabbits in which these values were relatively
high or low proved to be more susceptible to the growth of
the tumor implants. They also investigated the reactions of the
blood to the growth of transplanted cancer tissue. Their results
disclosed no appreciable change in hemoglobin concentration or
red blood cell counts for the early stages of tumor development.
Recently Blumenthal (3) reported the results of an investigation of the reaction of blood cellular elements to the growth
of neoplastic implants. Several types of tumors and both mice
and rats were utilized. He found, among other things, no significant change in the red cell count while the tumors were
comparatively small. Anemia developed after the tumors had
attained a large size and the animals had become debilitated.
A number of other papers might be cited since the reactions
of the blood to cancer have long been and still are a fruitful
field for research. But as indicated before, the relation of cancerous growth to the hemoglobin level has been generally regarded as secondary. Such data as can be found in the literature have been obtained in studies which were primarily conccrned with other aspects of cancer-blood relationships.
P r e l i m i n a r y w o r k in o u r l a b o r a t o r y i n d i c a t e d t h e
possibility ot~ a direct relation b e t w e e n t h e h e m o g l o b i n
level a n d n o t o n l y t h e early stages of cancer, b u t also
the chemically induced precancerous condition.
MATERIALS AND METHODS
All h e m o g l o b i n d e t e r m i n a t i o n s w e r e m a d e by t h e
m e t h o d d e s c r i b e d by E v e l y n u s i n g a n E v e l y n p h o t o electric c o l o r i m e t e r . T h i s t e c h n i c p r o v e d to be sensitive a n d t h o r o u g h l y reliable.
T u m o r i m p l a n t s . - - T h e m e t h o d of h y p o d e r m a t i c
i n j e c t i o n of finely d i v i d e d tissue w a s used. T h e t u m o r
tissue w a s f o r c e d t h r o u g h m u s l i n , t h e r e s u l t i n g m a terial p a s s i n g easily t h r o u g h a N o . i8 needle. E a c h
a n i m a l received o.o 5 m l . of this u n d i l u t e d h o m o g e n e o u s tissue s u b d e r m a l l y in t h e m i d - d o r s a l area
p o s t e r i o r to t h e cervical vertebrae.
M a m m a r y g l a n d a d e n o c a r c i n o m a s w h i c h h a d bec o m e stabilized by m a n y g e n e r a t i o n s of t r a n s p l a n t s
f u r n i s h e d t h e m a t e r i a l for t h e i m p l a n t s m a d e i n t o t h e
D b a g r o u p . T h e C 5 7 m i c e received p o r t i o n s of a
r o u n d cell s a r c o m a w h i c h h a d o r i g i n a l l y b e e n prod u c e d by t h e a c t i o n of m e t h y l c h o l a n t h r e n e in this
223
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Research.
Cancer Research
224
strain. Only animals without ulcers or any sort of
external lesions were included in the experiment. The
sarcoma implants used for the rats were also obtained
from a tumor induced by methylcholanthrene.
Cancer induction by butter yellow.--White rats of
the Wistar strain were fed on two basal diets, each of
which contained 0.6 per cent of dimethylaminoazobenzene (butter yellow) incorporated as a 3 per cent
solution in olive oil. Diet I consisted of Purina dog
chow, and diet 2 was cooked whole rice plus raw
carrots and salt.
Cancer induction by methylcholanthrene.--Dba and
C57 mice received single injections of o: 4 mgm. of
methylcholanthrene dissolved in 0.2 ml. of olive oil
subcutaneously in the right axilla.
TABLE I :
THE
EFFECT
OF" G R O W T H
OF T U M O R
Fig. 3 show clearly the striking decrease in hemoglobin
produced in rats when butter yellow (p-dimethylaminoazobenzene) was added to the diet. When the
basal diet was cooked whole rice and raw carrots, the
decrease in hemoglobin content was about 24 per cent
in 3 ~ days. At this period the liver of these animals
was macroscopically unaffected. Nodular cirrhosis affected the livers of most of the animals before the end
of the I48-day period. As the figure shows, the hemoglobin level remained almost constant after the initial
drop. With the development of hepatoma nodules, the
hemoglobin level fell below I I gm. per cent or 36 per
cent below normal.
The use of a nutritionally more complete basal diet
(Purina dog chow) led to an initial drop of about
IMPLANTS
ON TIIE
BLOOD
HEMOGLOBIN
Animals
Experiment
c
Strain
Number
1
Dba mice
15
Adenocarcinoma
2
Dba mice
14o
Adenocarcinoma
3
C 57 m i c e
4
Wistar
rats
Days after
implantation
Tumor
Tumor
size ~
7
14
21
$
0.5
1.5
3,o
7
14
21
CONCENTRATION
Hemoglobin
(gm. per
i o o ml.)
R e l a t i v e hemoglobin values f
( c o n t r o l s - ~oo)
15.1 -+- 0.7
1 4 . 2 -4- 0. 9
8 . 4 -4- 0 . 6
93.0
88.0
52.0
15.1
12.8
6.7
88.9
75.2
39.7
cm.
cm.
cm.
0.59 ccm.
3.85 ccm.
13.3 ~ c c m .
17
Sarcoma
20
2. 3
cm.
l O . 2 -4- 1.1
62. 5
6
Sarcoma
.-
4.5
cm.
9.5 -4- 2.5
55-7
* T h e v a l u e s f o r e x p e r i m e n t 2 w e r e o b t a i n e d b y m u l t i p l y i n g d i a m e t e r m e a s u r e m e n t s i n t h r e e d i m e n s i o n s d i r e c t l y . I n t h e o t h e r exp e r i m e n t s , t h e a v e r a g e d i a m e t e r s of m e a s u r e m e n t s in two d i m e n s i o n s o n l y a r e r e c o r d e d .
f T h e a v e r a g e h e m o g l o b i n v a l u e s of t h e a n i m a l s b e f o r e i m p l a n t a t i o n w e r e u s e d as c o n t r o l s .
E a c h a n i m a l r e c e i v e d o.o2 ce. of o r i g i n a l c a n c e r t i s s u e d i l u t e d to o.2 cc. w i t h s t e r i l e s a l i n e s o l u t i o n , i n s t e a d of t h e u s u a l
o.o5 co. of u n d i l u t e d t i s s u e .
RESULTS
CONTROL HEMOGLOBIN LEVEL
Ioc
|
Tumor imptants.--The decided drop in hemoglobin
level effected by the implantation of tumor tissue in
Dba mice is clearly shown in Table I and Fig. z. At
the end of the first week, the tumors were very small,
and the animals were vigorous and healthy; nevertheless, 7 to zo per cent hemoglobin decreases had occurred. This trend was continued during the second
week, and accelerated with time until death occurred.
The same general degree of effect was observed with
the sarcoma implants in C57 mice and Wistar rats.
Methylcholanthrene injections.--The results (Table
II, Fig. 2) show that a 4 per cent average drop in
hemoglobin had occurred in 22 Dba mice 5o days after
injection of the methylcholanthrene. That this drop
was real was borne ou t by the fact that the hemoglobin
level continued to fall to a level approximately xo per
cent below normal by the time 83 days had elapsed.
This same effect was observed with the C57 mice
which had received methylcholanthrene implants. No
visible tumors were evident at this time, but after I o3
days, 2z per cent of the animals showed visible tumors,
and the hemoglobin level had fallen to 84 per cent.
Effect of butter yellow and dict.--Table III and
~c
m
.J
X sc
z
~ ~,
-~ ~,
-r
lad
_ s~
\
\
o.1
i
i
\
240 EFFECT OF ADENOCARCI NOMA \b
.J
-IMPLANTS
ON H E M O G L O B I N
L E V E L 84: 14-0 D B A M I C E
3o
I. 4
6
8
io
iz
i
i
TIME IN DAYS AFTER IMPLANTATION
FIG.
I.
I2, 5 per cent in 3 ~ days. Thereafter the level remained
almost constant as far as has been observed (I62 days).
DISCUSSION
As the results show, there was a definite drop in the
hemoglobin level in the very early stages of the growth
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Research.
Taylor and Pollack--Hemoglobin Level
of tumor imi31ants. The data obtained from I55 mice
left little room for doubt on this point. Records on
2 5 mice for which the changes in hemoglobin level
were followed individually (although not reported
HEMOGLOBIN
CONTROL
(aO /o(
taJ
. j ~6
<
> q,,
225
an ever-decreasing hemoglobin level. Some mice
showed a fall in this respect from 17 gin. per cent to
less than 3 gin. per cent before death.
While factors other than the growth of the cancer
tissue may play a part in the extreme al~emia which
developed in the later stages, it is unlikely that such
an explanation could be reasonably advanced for the
initial moderate hemoglobin depression which accom-
LEVEL
I
_z ~4
I :ONTROL
HEMO,GLOBIN
LE'
t~
o c/i
...J
i.~ qc
(D
! - BUTT E I'(-YEL L.OW
PURINA
\1
-1-
->
D BUTTER-yELLOW
RICE-CARROT
\
tal 8~
\
841
I-<
_3 82
t.d
EFFECT OF METHYLCHO LANTHRENE."
INJECTIONS ON HEMOGLOBIN LEVEL
- - = D B A
a- 8a
MI
0S7
16
CE
,MICE
3o
e6
TIME
~o
do
go
"
4o
~
8o
i
qo
r
,oo
20
IN DAYS AFTER INJECTION
40
ExI)eriment
.
Mice
- Number
56
2.
160
laO
Dba
Per cent
hearing
visible
tumors
Ilemoglobin
(gin. p e r
J oo ml.)
Relative
hemoglobin
. values
( c o n t r o l s = IOO)
5o
o
1 5 . 6 ~--- 0 . 6
96.o
83
o
14. 7 --> 0. 7
9o.o
15.3 -t- I.O
90.2
14. 3 ~
84. 3
22
C57
19
BLOOD HEMOGLOBIN LEVEL OF TflE RAT
97
148
162
7
140
Days after
injection
TABLE III: T H E ]:7,FFt!,CT OF BUTTER YELLOW INGESTION ON THE
I.
120
FIG. 3
r~ ' ~
Strain
2 .......................
o
30
I00
T H E EFFECT OF SUBDERI~{AL DEPOSITS OF METHYLCI1OLANTIIRENE ON THE BLOOD HEMOGLOBIN CONCENTRA'FION
I .......................
T i m e on
diet, d a y s
80
TIME IN DAY,~
Fro. 2
TABLE II:
60
Number
of
animals
Average
weight,
in gin.
PURINA DoG C H O W - q - 0 . 6 %
9
9
9
9
9
9
154.4
171.8
176,3
18o.6
177.3
175.6
Hemoglobin,
gm. per c e n t
BUTTER YELLOW
15.4
13. 5
13.6
I4.4
14.1
14.4
- + 0-7
-+- 0.8
+ 0.8
+ 0.7
~--- 0.9
+----0.3
COOKED WHOLE RICE, RAW CARROTS~ ~ - 0 . 6 %
o
8
30
8
168.5
161.5
Relative
hemoglobin
' values
(controls=
zoo) *
lOO.O
82. 7
83.5
88.3
86.6
88.3
BUTTER YELLOW
16.3 • o.9
12.4 "+" 0.3
lOO.O
76.2
56
8
152. 7
I 2 . 1 --t- 0 . 6
74-5
97
148
I62
8
5
5
154.9
165.5
12-3 + O.7
1 2 . 0 + 0.5
12.3 --I- 0 . 6
75.6
73.6
75.5
165.7
* AI1 v a l u e s b a s e d on 1 6 4 gm. p e r cent o f h e m o g l o b i n as ~oo,
e x e e p t for the first v a l u e reported, w h i c h w a s based on 1 5 . 4 gm.
per cent. I n rats of that age a n d size the h e m o g l o b i n level is still
rising.
individually here) manifested in each individual case
a decline in the hemoglobin concentration even before
the tumors were large enough to be measured. The
later stages of tumor development were associated with
84
o
lO 3
21
1.2
panied the early development of the tumor. The
animals at this time appeared vigorous and unimpaired.
The hemoglobin reaction to the methylcholanthreneand dimethylaminoazobenzene-produced precancerous
states was also striking in its uniformity. The effect
of the methylcholanthrene deposits on the hemoglobin
level appeared to be not unlike the effect in this regard
of the genetically determined influence which Strong
(I9) reported as operating in cancer-susceptible mice.
It might well be that the two phenomena are closely
related, perhaps differing mainly in the intensity of
the carcinogenic stimulus which of course is more
intense in mice receiving the chemical.
It is especially worthy of note that the cancerresistant and the cancer-susceptible mice reacted in the
same manner to the treatment with methylcholanthrene. As the results show, a group of C57 black
mice and a group of Dba mice each manifested a
hemoglobin depression of IO per cent by about the
8oth day, before visible tumors had appeared, after
receiving the methylcholanthrene deposits. A carcinogen of this type is so powerful that genetic influences tend to be nullified.
The effect of butter yellow ingestion on the blood
hemoglobin of rats probably involves some factors not
present in the action of methylcholanthrene. As the
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Cancer Research
226
data show, the hemoglobin in this instance dropped
suddenly to a new level and then remained constant
until the appearance of hepatomas at which time a
further drop was recorded. Liver damage does not
seem to be a satisfactory explanation since the livers
at the 3c-day period were macroscopically normal,
while in the later period severe cirrhosis developed.
However, the hemoglobin concentration remained
stabilized at the new level and was apparently unaffected by the progressive damage to the liver tissue.
As time went on, there was actually less individual
variation in the hemoglobin levels of the individual
rats in this experiment.
In this connection, it was significant that a diet (ricecarrot) k n o w n to favor the development of liver carcinoma in the presence of butter yellow also effected a
more severe decline in the hemoglobin level.
Rats, fed butter yellow, which developed hepatomas
did not manifest the extreme anemia which was
characteristic of the late stages of external tumors.
Subdermal implants of adenocarcinoma may attain a
comparatively large size before killing the animal;
sometimes as m u c h as 2o gin. of tumor tissue develops
in a 3 ~ gm. mouse. Under such circumstances the
hemoglobin level may be depressed 85 per cent below
normal. Obviously, a liver tumor would cause death
long before attaining any such size and, accordingly,
the late stages of hepatoma tend to depress the hemoglobin level to a lesser extent; i.e., about 3 6 per cent
below normal.
T h e underlying mechanism responsible for the resuits reported here must necessarily remain obscure
until this aspect of the problem has been thoroughly
investigated. However, it does seem permissible,
especially in view of Craig's and Greenstein's work
(8, io) referred to before on the effect of cancer on
cytochrome C and catalase, to postulate an antagonistic
action between hemoglobin and cancerous tissue, and
to a lesser extent precancerous tissue. As far as the
precancerous condition is concerned, it seems probable
that one of the characteristics of cancer tissue which
is gradually assumed by the ceils undergoing transformation is that of incompatibility with high hemoglobin levels. It is likely that this is true of mice which
have a tendency towards spontaneous cancer as well
as animals under the influence of applied chemical
carcinogens.
SUMMARY AND CONCLUSIONS
i. Evidence based on results obtained from a study
of i55 tumor implants in mice indicated that tumor
tissue has an antagonistic action toward the blood
hemoglobin of the host. T h e hemoglobin level was
depressed by the time the implant had grown to
measurable size and thereafter became progressively
lower until death occurred.
2. T h e precancerous condition as induced by methylcholanthrene was associated with a gradual fall of
hemoglobin values which began soon after the mice
received injections of this chemical and continued on
into the cancerous condition. T h e hemoglobin of
cancer-susceptible and cancer-resistant mice behaved in
the same m a n n e r to this carcinogen. It was concluded
from these results that precancerous tissue was chore or
less antagonistic to hemoglobin in the degree to which
it approached the cancerous state.
3. Ingestion of butter yellow by rats induced a
sudden drop in the hemoglobin to a new level by the
3oth day of the experiment. Thereafter the hemoglobin
concentration remained fairly constant until hepatomas
developed, after which a further decline was noted.
T h e h e m o g l o b i n of butter yellow-fed rats dropped to a
m u c h lower level (7 6 per cent) on a rice-carrot basal
diet then on a Purina dog chow basal diet (83 per
cent). Increasing liver damage as manifested by the
appearance of cirrhotic nodules did not effect any
further change in the hemoglobin level over a 162-day
period.
We wish to acknowledge the invaluable assistance and encourageInent of Professor Roger I- Williams, Director of the
Biochemical Institute. Our thanks are also due to Mrs. Dorothy
Pennington and Miss Juanita Thacker for technical assistance
rendered during the course of this research.--A,thors.
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Correction
See: Kensler, C. J,, S. O. Dexter, and C. P. Rhoads. T h e
Inhibition of a Diphosphopyridine Nucleotide System by
Split Products of D i m e t h y l a m i n o a z o b e n z e n e . Cancer Research, 2 : i - i o . i942.
In the graphic f o r m u l a for the split p r o d u c t of comp o u n d III in Fig. 7, P. 9, the m e t h y l group s h o w n in the
ortho- position should be in the meta- position.
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Research.
Hemoglobin Level and Tumor Growth
Alfred Taylor and Maxwell A. Pollack
Cancer Res 1942;2:223-227.
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