Download Cancer andHuman Liver Catalase

Cancer and Human Liver Catalase*
EDWARDE. MASON,TING-FONGCHIN, YAOW. Li, ANDSIDNEYE. ZIFFREN
(Department, nf Surgery, Stale University of Iowa, College of Medicine,
lou-a City, loica)
SUMMARY
Data presented in the present paper indicate that human liver catalase depression is
related to weight loss. A statistical study was first made to determine the catalase
activity in correlation of the iodotitrimetric and spectrophotometric methods for
biopsy and autopsy samples from cancer and cancer-free patients. Cancer patients had
a 22 per cent lower liver catalase activity than cancer-free patients. A two-by-two
factorial analysis of variance comparing presence or absence of cancer and weight loss
revealed that weight loss accounted for the catalase depression and that, when correc
tion was made for the weight loss effect, no additional cancer effect was seen. Distribu
tion of catalase in subcellular fractions was also studied and failed to show any sig
nificant cancer effect but did demonstrate the relationship between weight loss and
catalase depression in the soluble fraction. No effect of sex was observed, which is con
sistent with Adams' observations in laboratory animals that, when the male of a
species does not show an increased liver catalase as compared with female, no sig
nificant depression of liver catalase is observed (2).
Studies of liver catalase depression by cancers
of men were pioneered in 1910 by Blumen thai and
Brahn (6). They reported that the liver catalase
activity was very low in human beings who had
died as a result of various forms of cancer. Experi
mental work prior to 1941 has been summarized by
Greenstein (11) and has amply demonstrated that
the peroxide-splitting enzyme, catalase, is con
siderably reduced in the liver of some strains of
mice and rats bearing tumors. The decrease in
liver catalase in susceptible animals is progressive
with the growth of the tumor. There have been re
ports that in some strains of animals depression of
catalase did not occur despite rapid tumor growth
to a large size (4). When an effect is observed the
tumor must grow rapidly and reach a size equal
to 5 per cent of the animal's total body weight
before the effect can be detected (10).
Recently Nakahara and Fukuoka (15) isolated
a heat-stable, protein-like catalase-depressing
material from human tumors and demonstrated
its effect in mice. Nakagawa (14) has isolated a
liver catalase-depressing substance from the urine
* This work was supported by the J. B. Phillips Memorial
Grant for Cancer Research from the American Cancer Society.
Appreciation is expressed to Prof. E. F. Mason for proofreading
and checking of statistical calculations.
Received for publication May 4, 1960.
of a cancer patient and the gastric juice of patients
with stomach cancer. A comparison between the
liver catalase activity of patients with malignant
tumors and patients with gastric or duodenal ulcer
was reported in 1958 by Kiyota (13). They found
a lower catalase activity in the cancer patients
but did not evaluate the possible nonspecific ef
fect of poor nutrition. A nutritional effect in liver
catalase activity of animals has been reported by
Van Pilsum (17) in 1957. The specificity of de
pression of liver catalase due to cancer in man is
therefore still open to question, since malnutrition
alone could cause the mild depression observed. It
has also been observed by Adams (1) that only the
liver catalase of animals which is increased by
testosterone is depressed by cancer.
The present work was undertaken in three
rather distinct phases. Initially an investigation
was made to find out whether there was any differ
ence between patients with cancer and patients
who were operated upon for noncancerous condi
tions. At the same time the methods used were
evaluated for reliability. Secondly, another im
portant factor was examined, namely, the presence
of a greater frequency and per cent of weight loss
in cancer patients as compared with noncancer
patients. This was an amplification in which a twoby-two factorial analysis was used, and the two
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MASON et al.—Cancer and Human Liver Catatase
variables, cancer-no cancer and weight loss-no
weight loss, were subjected to an analysis of
variance
after an accumulation
of sufficient
replications of appropriately
selected patients to
provide equal numbers of patients in each of the
four groups. Finally, the distribution
of human
liver catalase in the subcellular fractionations was
investigated in relation to the effect of cancer and
weight loss. Also, an analysis was made of the
relationships
between the human liver catalase
activity and sex. All these findings are consistent
with experimental
work in certain strains of
animals in which liver catalase is not directly in
fluenced by cancer. The analysis of data leading to
this conclusion and the interpretation
of these
findings comprise the following presentation.
EXPERIMENTAL
AND RESULTS
PART A
A study of arithmetic means and variations of
liver catalase activity in cancer and noncancer
patients as compared with the statistical cor
relation of two analytical methods
Selection of patients and samples.—Liver bi
opsies were obtained from patients whose opera
tive procedure involved exposure of the upper
abdomen. Livers from autopsies were obtained
when patients were examined within 6 hours of
death. Samples were obtained from patients who
did not have primary liver disease and from areas
containing no metastatic
tumor. The specimens
were chilled immediately and taken to the labora
tory, where a 5 per cent homogenate was prepared
in 0.05 M phosphate
buffer at pH 6.8 with a
Potter-Elvehjem
homogenizer
surrounded
by
crushed ice.
Methods used in analysis.—
1. The titrimetric
method
used for these
studies is a modification of the method of Sumner
and Dounce (7). A 0.05-ml. aliquot of the 5 per
cent homogenate was added to 50 ml. of 0.1 M
hydrogen
peroxide buffered with a 0.0067 M
phosphate buffer at pH 6.8 and in an ice-cooled
beaker. Stirring was done with a Teflon-covered
magnet in a moving magnetic field. Samples of
5 ml. volume were withdrawn from the reaction
chamber at 0, 1,2, and 3 minutes and injected into
5 ml. of 2 N sulfuric acid. To each of the samples
10 ml. of 10 per cent potassium iodide and 1 drop
of 1 per cent molybdic acid were added. Exactly
3 minutes after the addition of the iodide, titration
was carried out with 0.005 M thiosulfate, with a
few drops of starch added toward the end of the
titration to improve the end-point. A constant
artificial lighting was used, since sunlight was
observed to affect the titration.
1475
2. For the spectrophotometric
method (5) a
Beckman Model DU spectrophotometer
was used
with 1-cm. light path quartz cuvettes. The rate of
disappearance of hydrogen peroxide was measured
at 240 imi by change in optical density. As a pre
liminary step, two cuvettes were prepared with 3
ml. of an appropriately dilute homogenate in 0.5 M
phosphate buffer of pH 6.8. At zero time 1 ml. of
a 3.5 X 10~2M solution of hydrogen peroxide in
buffer was added to one of the cuvettes and 1 ml.
of buffer was added to the other as a blank.
Optical density measurements were then taken at
10-second intervals for 4 minutes. The unit of
catalase activity used is defined by this equation:
TT
¿»3
*
Id
r /-l-l
U is the unit of catalase activity per minute per
gram of fresh liver sample.
I0 is the initial concentration of the thiosulfate.
It is the concentration
of the thiosulfate
at t
minutes.
T is reaction time in minutes.
C is the concentration of homogenate.
From Table 1 the mean catalase activity for the
seventeen biopsy samples was found to be 22.5 per
cent lower in cancer patients than in the patients
having no cancer. The correlation between these
two methods in 24 samples (autopsy included) was
0.90. It was 0.79 in the seventeen biopsy samples.
This indicates a high degree of correlation between
these two methods. Although the correlation is
higher when the autopsy data are included, the
correlation coefficient of 0.79 was sufficiently high
in the biopsy data to warrant use of either method
for studies of catalase activity in human liver
samples obtained from living patients with and
without cancer. Subsequent analyses were there
fore carried out with the titrimetric method alone.
PART B
Comparison of cancer and weight loss as they
relate to liver catalase activity with use of
a two-by-two factorial analysis
In Part A we found that the liver catalase
activity was 22.5 per cent lower in the cancer
patients than in the patients having no cancer.
The question remained as to the cause of this de
pression in cancer patients. Body weight loss was
often present as an evidence of poor nutrition. To
determine the relationship of liver catalase activ
ity to body weight loss and to cancer, the patients
were divided into four groups. These groups of
patients were selected as having: (a) less than 10
per cent body weight loss and no cancer, (b) more
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1476
Cancer Research
than 10 per cent body weight loss but without
cancer, (c) less than 10 per cent body weight loss
with cancer, and (¿)more than 10 per cent body
weight loss with cancer. Determination of body
weight loss was by the history recorded in the
patient's hospital record. This usually consisted of
both the "present" and "usual" weight and the
absolute weight loss plus the time interval of
weight loss. Because of variations in body build,
obesity, and duration of weight loss, it was con
sidered desirable to simply divide the patients
into groups as they fell above or below an arbi
trary 10 per cent body weight loss and thus to
consider weight loss as a categorical rather than
an ordered variable. The procedures for the
biopsy collection and homogenate preparation
were the same as in Part A, but only the iodotitrimetric method was used for determination of
catalase activity. Some data from the earlier study
were used, as indicated by the identical patients'
numbers in the tables. The additional patients
Vol. 20, November
1960
were selected preoperatively on the basis of pres
ence or absence of cancer or body weight loss, as
was required to supply an equal number of reitera
tions in the deficient groups for the projected twoby-two factorial analysis.
The data used for the analysis of variance are
shown in Table 2, and the actual analysis is shown
in Table 3. It is assumed that these are random
samples from a normal population and that the
variance is the same for each portion of this normal
population. There are two columns in which
cancer and noncancer patients are compared and
two rows wherein weight loss and no weight loss
are compared. The final analysis culminates in an
F value of 4.25 with which these statistics must be
compared to determine their significance. F
.95 (1,20) = 4.25 (8) indicates that if any of the F
ratios are greater than 4.25 they are significant
at a confidence level of 95 per cent. It is, there
fore, apparent that the two-row means with an F
ratio of 10.67 were significantly different, or in
TABLE1
DATAFORCOMPARISON
OFLIVERCATALASE
ACTIVITY
IN CANCER
ANDCANCER-FREE
PATIENTS
wtBody
Caseno.12345(i789101112131415161718192021222324Age6154466250807768717049687954597378837836812«8282SexMMFMFMFMMFMMFMFMMMFFMMMMPATIENTS'Tumor
wt.0.260.530.7500.0000.10¿02050Ã
wt.001.55Ó3163819•j1102231018?tttttDiagnostaPeripheral
diseaseGastric
vascular
ulcerDuodenal
ulcerDuodenal
ulcerCholecystitisDuodenal
ulcerMean
noncancerGastric
of biopsies,
±44205131145153213162133ins261214170*1
±37202122192187230194158
carcinomaEsophageal
carcinomaEsophageal
carcinomaRectal
adenocareinomaColonie
carcinomaAbdominal
carcinomatosisGastric
carcinomaPancreatic
carcinomaPancreatic
carcinomaGastric
carcinomaGastric
carcinomaMean
302.503.00WENTIFICATIONWt.l«sBody
cancerArteriosclerosisAcute
of biopsies,
tracheobronchitisMultiple
abscessesHip
diabetesBacterial
fracture,
endocarditisMean
noncancerGastric
of autopsies,
4710142*72
+
cancerUrinary
cancerMean
bladder
+ 37
+ 42ACTIVITYSpectro-photometric2282
of autopsies, cancerCATALASETitrimetric221323231280231205*249
* Arithmetic mean of groups ±standard deviation (root mean square deviation),
t Autopsy samples.
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MASON et al.—Cancer and Human Liver Catalase
other words there was a relationship between
weight loss and liver catalase activity. The column
means representing a comparison between cancer
and noncancer were not significantly different.
Since only weight loss had an effect, no inter
action between weight loss and cancer was to be
expected, and none was found.
PARTC
Subcellular distribution of catalase in patients
with the variables cancer-no cancer and
and weight loss
Although we can be 95 per cent sure that a
relationship between weight loss and liver catalase
does exist, a statement that cancer does not
specifically cause a decrease in liver catalase can
not be made with the same degree of confidence.
This is inherent in the nature of the statement and
in the statistical methods. All one can say is that
no relationship could be found. Because it is gen
erally believed that toxohormone does depress hu
man liver catalase, it seems important to look for
such an effect by making use of a more sensitive
experimental technic. Since the soluble (nonparticulate, nonsedimentable) catalase is reported
to be the only portion of liver cell catalase de
pressed early and by the smaller tumor growths
in laboratory animals (2, 3, 18), an investigation
was made of the activity distribution of catalase
in subcellular fractions of human liver, again in
cluding patients selected with the variable cancer
and weight loss for study.
In this experiment a PVP'-sucrose buffer
medium (19) (10 per cent polyvinylpyrrolidon
and 20 per cent sucrose, at pH 6.8) was used for
homogenization, and 0.1 per cent triton-XlOO
was added after fractionation to assure dissolution
of all the catalase-containing particles. The 5 per
cent homogenate was centrifuged at a speed of
IS.OOOX? for 30 minutes. The two fractions
were then separated, and each was made up to
the original volume. The titrimetric method was
used for determination of catalase activity in the
whole homogenate and in each of the fractions.
The data indicating the distribution of human
liver catalase activity are shown in the Table 4.
Table 4 shows no cancer-specific depression of
either the soluble supernatant catalase or the sedimentable particulate catalase. Recovery was only
90.7 per cent in the patients who had both cancer
and weight loss. The instability of the enzyme
seemed to be slightly greater in the sediment than
in the supernatant. An analysis of variance was
1PVP donated by Farbenfabriken Bayer AG, Germany:
molecular weight about 70,000.
1477
carried out with the data from column C (Table 4)
and again showed a significant (90 per cent confi
dence) relationship between weight loss and
catalase activity but no evidence of a selective or
specific tumor-produced agent which actively de
pressed the soluble portion of human liver catalase.
The combination of cancer and weight loss was
associated with a higher mean soluble catalase
level—96—thanwas seen in patients with weight
loss and no cancer—-88.These figures are not sig
nificantly different and cannot be used to prove
that cancer increases liver catalase in patients
with weight loss, but they do support the earlier
finding that cancer has no significant depressive
effect on the catalase of human liver.
A Mocancer biopsy
A Cancer biopsy
O No cancer autopsy
•Cancer autopsy
40
80
120
160 200
240
Units by Tilrimetric Method
280
320
CHART1.—Aplot of biopsy and autopsy data for cancer
and cancer-free patients with the titrimetric method on the
abscissa and the spectrophotometric method on the ordinate.
Since the correlation coefficient, r = \/b b', where 6 and 6'
are estimates of the regression lines of K on A' and X on Y,
these regression lines were drawn with the biopsy data used
alone (r = 0.79) and for all the data (r = 0.90).
In those strains of laboratory animals which
show no depression of liver catalase by cancer
there is also no difference in catalase activity be
tween the two sexes (2). Cancer-free patients from
the present study were, therefore, paired accord
ing to weight loss into male and female groups. It
was hypothesized that the means of the two
populations are equal, and this was tested with the
statistic "t" (8) :
Zi(male)
- X2 (female)
+ U/AT2)
,-2)
-2)
= -2.179;
= +2.179
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1478
Cancer Research
Since the observed t fell between the limits ex
pected when an a of 0.05 was used, there is no
reason to doubt that men and women have the
same level of liver catalase activity.
DISCUSSION
The above experimental data suggest that
cancer depresses human liver catalase indirectly
through the malnutrition produced in the host.
That the liver catalase activity in cancer patients
is usually lower than in cancer-free patients is con
firmed by Part A of the present study, but the
cause of the lowering cannot be assigned to a
Vol. 20, November
1960
specific effect of cancer. Usually cancer is ac
companied by weight loss, as is illustrated in Part
B of this study. The patients having more than 10
per cent body weight loss but without cancer
showed a significant lowering of liver catalase.
By contrast, the patients with cancer but without
weight loss showed no significant liver catalase
depression. As a result of these analyses which
take into consideration the additional variable,
weight loss, it is necessary to reject the hypothesis
of Blumenthal and Brahn and of Kiyota, neither
of whom considered body weight loss.
From these results, a new hypothesis is sug-
TABLE 2
DATAOFLIVERCATALASE
ACTIVITY
INPATIENTS
CLASSIFIED
ACCORDING
TOPRESENCE
ORABSENCE
OFCANCER
ANDWEIGHTLoss
IDENTIFICATIONCase
PATIENTS*
lossBody
wt.DiagnosisCATALASE
no.AgeSexWt.
ACTIVITY
Group 1—< 10% body weight loss and no cancer
5i1Ì52627505461586649FMMMMM000000060709Group
ulcerPeripheral
diseaseGastricvascular
ulcerDuodenal
ulcerPeptic
ulcerMeanweight
3822023923116117896*188
+
body28293303132485546844949MMFMMF111215162234CholecystitisGastric
2—> 10%
cancerGastric
loss but without
ulcerDuodenal
ulcerDuodenal
ulcerPyloric
obstructionObstructed
stomachAbdominal
anginaMean231323221237228256*249
+ 52
Group 3—< 10% body weight loss with cancer
carcinomaColonie
331114343515744954737759MMMMFF(100103050609Group
carcinomaPancreatic
carcinomaGastric
carcinomaColonie
carcinomaPancreatic
carcinomaMeanbody
10%3616913378487371795968FMMFFM171819223038Gastric
4- >
cancerColonie
weight loss with
carcinomaGastric
carcinomaEsophageal
carcinomaGastric
carcinomaGastric
carcinomaEsophageal
cancerMean166213183232•220261*213±34166214145133204131»166
+ 35
' See footnote *, Table 1.
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MASON*et al.—Cancer and Human Lirer Catatase
gested—that cancer has a very mild (if any) specific
effect on human liver catalase activity. This does
not mean that human cancers do not produce toxohormone, since Nakahara and Fukuoka have iso
lated a catalase-depressing material, toxohormone,
from human tumors and demonstrated its effect in
mice. From Adams' series of papers it appears
that in susceptible strains of animals the action of
the specific cancer-produced, liver catalase-inhibiting material is to interfere or compete with
the testicular and adrenal hormones in their
stimulation of increased catalase production. If a
strain of animals has the same liver catalase
activity regardless of the level of testicular and
adrenal hormones, then no cancer catalase-de
pressing effect is to be expected. The human sub
ject, showing no sexual difference in liver catalase
activity, is like those strains of laboratory animals
in which liver catalase is not susceptible to de
pression by toxohormone.
Additional support for this new hypothesis was
found in the study of the distribution of human
liver catalase in subcellular fractions. Price (16)
points out that, if cancer affects liver catalase, the
distribution will vary in fractions from cancer as
compared with cancer-free animals. He observed
that the insoluble fraction was not reduced in the
liver of tumor-bearing animals, whereas the
catalase of the soluble fraction was reduced to
1479
less than one-third that found in the correspond
ing fraction from normal liver. In our experiment,
we found no significant effect of cancer on the
distribution of human liver catalase.
In a later paper Price (9) showed that the ap
pearance of activity in the soluble fraction of mice
was an artifact, since in the PVP-sucrose medium
80-99 per cent of the activity was in the particulate fraction, depending on the pH of the homogenate. When catalase was obtained directly from
the isolated part ¡culatea uniformly high specific
activity is found. There is less enzyme in the liver
of tumor-bearing animals, but qualitatively it is
identical to that found in normal animals. Adams
recently has again raised the question of distribu
tion of catalase and gives data to indicate that
there is a decrease in permeability of the mem
brane (3) of catalase-containing particles as a re
sult of cancer. It was because of these reports that
fractional studies were undertaken and that PVPsucrose medium was used. Since approximately
50 per cent of human liver catalase was found as
soluble, nonparticulate catalase, additional com
parative studies were carried out in other species
with the same homogenate medium and conditions
(such as pH, centrifugal force, time and tempera
ture for homogenization, etc.) The results were
most interesting and will be reported in detail in a
separate paper; there was a striking difference in
TABLE 3
STATISTICAL
ANALYTICAL
DATAOFHUMAN
LIVERCATALASE
ACTIVITY
IN
TWO-BY-TWO
FACTORIAL
ANALYSIS:
CANCER-NO
CANCER
ANDBODY
WEIGHT
Loss-No BODYWEIGHTLoss
A: DATA OF TOTAL»
cancer1,496
< 10% body
loss
weight lossNo.
> 10% bodyweight
0
1,126.02,622.0Cancer1,276.0
¿.11904,891.0
994.02,270.0Tot»!2,772.0
B: ANALYSISOF VARIANCE;
squares17,670
of
How means
Column means
InteractionSubtotalWithin
groups
squnre17,670
rati«10.67
5,400
5,400
1
3.27
4301,652K 0.20F
49023,50033 132023Mean
,05056.550D.f.*1
95 il, 20)
= 4.35
TotalSum
* Degrees of freedom.
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1480
Cancer Research
Vol. 20, November
1960
the distribution of catalase in the liver cells of formation, and other substances are probably also
different species. In our own laboratory 97 per essential.
cent was sedimentable in mice at 18,OOOX<7, In conclusion, human liver catalase did show
compared with 50 per cent in man. There was also a demonstrable depression by cancer, but it can be
an inactive sedimentable fraction which varied explained on a nonspecific basis. The distribution
greatly among species and was released or acti
of catalase in human liver was different than in
vated by triton-XlOO.
toxohormone-responsive animals. There was no
The relationship of body weight loss and liver sexual difference in liver catalase activity in man.
These latter two findings help to correlate the find
catalase depression observed in this study is prob
ably due to malnutrition. Nutritional effects have ings in man and those in experimental animals.
been documented in the laboratory animal. Iron, Although human liver is relatively insensitive to
magnesium, copper (12), isoleucine, tryptophan,
toxohormone, this does not invalidate the finding
and phenylalanine (17) are all essential to catalase of others that toxohormone is produced by human
TABLE 4
SUBCELLULAR DISTRIBUTION' OF LlVER CATALASE IN CANCER-FREE AND CANCER PATIENTS
COMPARED
WITHBODYWEIGHTLoss
IDENTIFICATIONCaseAgeSexWt.
PATIENTS'
ACTIVITYOrigi
nal
ment
homog18000
XICSTATISTICSDistribution5
—— XIOO
18000X»BSupernatant
enate
xiooAXIOO
A
ASedi
ARecoveryB+C
lo»«Body
wt.DiagnosisCATALASE
Group 1—<10% body weight loss
stoneGall
bladder
38394041425835714964FFFMF00099Gall
stonesGall
stonesPeptic
ulcerPyloric
obstruction256265248244261115130142138132139131129107114«124
+ 134549575150*505449524444*49999910»9594*99
Group 2—>10% body weight less
ulcerGall
43444546474857497749MFMMF11U151734Gastric
stonesObstructed
bladder
stomachPseudo
tumorSuperior
mesentericartery
occlusion1992951632148987162761193497121768959»88
±234358465539*484941474267*4992999397105*97
Group 3—< 10% body weight loss
cancerGastric
48495051525874647759MMFFM00355Pulmonary
carcinomaPulmonary
carcinomaColonie
carcinomaColonie
carcinoma3751472422032121367314711110021768105105109»121
+ 183650615547»505846445153*509496104106101•100
10%Gastric
4—>
carcinomaGall
53545556577063794876FMFFM1216161727Group
carcinomaPulmonary
bladder
carcinomaColonie
carcinomaGastric
carcinomabody
loss24718018415726512791055093103728685132»96
weight
+ 235151523335*444240475550»479391988785»91
* Arithmetic mean of groups + standard deviation.
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MASON et al.—Cancer and Human
Lirer Caialase
1481
TABLE 5
STATISTICAL
ANALYTICAL
DATAOF HUMANLIVERCATALASEACTIVITY
IN SOLUBLEFRACTION(SUPERNATANT)
IN TWO-BY-TWOFACTORIAL
ANALYSIS:
CANCER-NOCANCERANDBODYWEIGHTLoss-No BODY
WEIGHTLoss
A. DATA OF TOTALS
cancer620
< 10% body weight loss
> 10% body weight lossNo.
4411,061Cancer6044781,082Total1,224
9192,143
B. ANALYSISor VARIANCE
squares4,651
of
Row means
Column means
InteractionSubtotalWithin
square4,651
23
1131619Mean23
1394,81317,75022,563D.f.1
1391,109F
groups
ratio4.2
0.02
0.10F
.90 (1, 16)
= 3.07
TotalSum
cancers. The mechanism of toxohormone produc
tion and action remains a challenge in the human
cancer problem.
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Effect of Tumor Tissue upon the Hormonal Control
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2.
. Sex Differences in Tissue Catalase Levels, and
Their Relation to the Catalase Depressing Action of Tu
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3.
. The Effect of Sarcoma 37 on the Intracellular Dis
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D.; SKAVINSKI,E. R.; and STEIN,A. M. Cata
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F., and BRAUN,B. Die Katalasewirkung in
normaler und in carcinomatoser Leber. Ztschr. Krebsforsch., 8:436-40, 1910.
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Cancer and Human Liver Catalase
Edward E. Mason, Ting-fong Chin, Yao W. Li, et al.
Cancer Res 1960;20:1474-1481.
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