Folia Medica 2013; 55(2): 51-57

Copyright © 2013 Medical University Plovdiv

doi: 10.2478/folmed-2013-0017

ORIGINAL ARTICLES

Experimental Investigations
EFFECT OF TESTOSTERONE PROPIONATE ON ERYTHROPOIESIS AFTER
EXPERIMENTAL ORCHIECTOMY

Delyan P. Delev1*, Delyana P. Davcheva2, Ilia D. Kostadinov1, Ivanka I. Kostadinova1

1Department of Pharmacology and Clinical Pharmacology, 2Department of Clinical Laboratory, Faculty of
Medicine, Medical University, Plovdiv, Bulgaria

ABSTRACT
INTRODUCTION: Androgen deficiency anemia occurs most frequently in pharmacogenic sup-
pression of androgen synthesis or with advancing age in men. Bilateral orchiectomy is a
surgical modality used in the treatment of metastatic prostate carcinoma. It is accompa-
nied by marked decrease in circulating serum levels of androgens.
AIM: The aim of the experimental study was to determine the effect of substitution therapy
with testosterone propionate (TP) on some haematological parameters of erythropoiesis in
male rats after orchiectomy.
MATERIAL AND METHODS: Eighty Wistar male rats with mean weight of 252.3 g were used
in the study. The animals were allocated into 2 control orchidectomized groups, 2 sham-
operated groups and 4 experimental orchidectomized groups. Testosterone propionate was
administered intramuscularly, once a week at a dose of 4 mg and 8 mg per kilogram of
body weight for 15 days and for 15 weeks. Erythrocyte count was performed and hemo-
globin and hematocrit levels were measured.
RESULTS: In the chronic experiment there was a significant decrease in red blood cells and
hemoglobin, and a tendency of decrease in hematocrit after orchiectomy. The effect of TP
on erythropoiesis in orchiectomised rats is dose-dependent.
CONCLUSION: TP replacement therapy in doses of 4 mg/kg and 8 mg/kg has a stimulating
effect on erythropoiesis only in chronic administration.

Key words: testosterone propionate, erythrocytes, hemoglobin, hematocrit, experimental

andropause

INTRODUCTION
experimental model of heart failure testosterone
Male climacteric is a term used first in 1939 to improves cardiac function and mobilizes bone
describe the physiological changes occurring in marrow stem cells.6 Indications for treatment were
men after the age of 50.1 They are associated with aplastic anemia7, and renal failure8. Testosterone
decreased libido, mood swings, reduced muscle plays an important role in circadian rhythm of
mass and strength, increased visceral fat, reduced bone marrow function in adult rats.9 Reduction of
bone mineral density etc.2 Similar changes occur in normal serum testosterone levels is associated with
young men with androgen deficiency. With advanc- suppression of erythropoiesis. It has been found in
ing age, the levels of testosterone, produced by the most experimental and case-control studies of tes-
Leydig cells, decline progressively in elderly men3 tosterone treatment in elderly men that it stimulates
and rats4. erythropoiesis and increases hematocrit 3% - 5%
Androgens affect erythropoiesis.5 They were above the normal range. High hematocrit values
used as major pharmacological agents to stimulate (55% - 60%) lead to a significant increase in blood
erythrocyte production before the introduction of viscosity. Erythrocytosis during testosterone therapy
recombinant hematopoietic growth factors. In an has been found in 6% to 25% of adult individu-
*Correspondence and reprint request to: D. Delev, Department of Pharmacology and Clinical Pharmacology,
Faculty of Medicine, Medical University, Plovdiv; E-mail: delevg@gmail.com; Mob.: +359 888 713 731
15A Vassil Aprilov St., 4002 Plovdiv, Bulgaria
Received 12 February 2013; Accepted for publication 28 February
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| 203.56.241.2
51
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D. Delev et al

als.10 Erythrocytosis occurs both in parenteral and MATERIAL AND METHODS

enteral administration and it is less frequent when
transdermal therapeutic agents are used.11
Despite abundant clinical data changes in the
concentrations of sex hormones that have hemor-
heological consequences 12, have not been well
studied in a model with orchiectomy. It is known
that hemorheological parameters show gender
differences that might be altered by experimental
bilateral orchiectomy.13
AIM
The aim of the present experimental study was to
investigate the effect of testosterone propionate
on the level of erythrocyte count, hemoglobin and
hematocrit in conditions of acute and chronic treat-
ment of male orchiectomised rats.
The study included 80 male Wistar rats with a mean
weight of 252.3 g. The design of the experiment
was approved by the Bulgarian Food Safety Agency
(license No 21 of 19.03.2012) and by the Ethics
Committee at the Medical University of Plovdiv
(protocol No 3 of 25.07.2012). All animals were
divided into groups (Table 1) and treated as shown
in Table 2.
ORCHIECTOMY OF MALE RATS
General anesthesia was performed with midazolam
(Dormicum, Roche) (2.5 mg/kg bdw i.p.) and fen-
tanyl (Fentanyl, Richter-Gedeon (0.25 μg/kg bdw
i.p.). After the anesthesia the animals fell soundly
asleep and woke up after 20 ± 2 minutes.
A 10-mm-long skin incision was made on the
scrotum apically. The incision was extended 5

Table 1. Description of the groups in the experimental study

Group Abbreviation Description

1 SOAC Sham operated 6-month-old animals in acute treatment

2 COAC Control group of 6-month-old orchiectomized rats in acute treatment
3 О4AC Orchiectomized 6-month-old testosterone treated rats (4 mg/kg b.w.) in acute treatment
4 О8AC Orchiectomized 6-month-old testosterone treated rats (8 mg/kg b.w.) in acute treatment
5 SOCHR Sham operated 6-month-old rats in chronic treatment
6 COCHR Control group of 6-month-old orchiectomized rats in chronic treatment
7 O4CHR Orchiectomized 6-month-old testosterone treated rats (4 mg/kg b.w.) in chronic treatment
8 O8CHR Orchiectomized 6-month-old testosterone treated rats (8 mg/kg b.w.) in chronic treatment

Table 2. Experimental protocol

Group Abbreviation n Treatment Duration

1 SOAC 10 0.5 ml Oleum helianti 15 days

2 COAC 10 0.5 ml Oleum helianti 15 days
3 04AC 10 4 mg/kg b.w. testosterone propionate 15 days
4 O8CHR 10 8 mg/kg b.w. testosterone propionate 15 days
5 SOCHR 10 0.5 ml Oleum helianti 15 weeks
6 COCHR 10 0.5 ml Oleum helianti 15 weeks
7 O4CHR 10 4 mg/kg b.w. testosterone propionate 15 weeks
8 O8CHR 10 8 mg/kg b.w. testosterone propionate 15 weeks

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 Effect of Testosterone Propionate on Erythropoiesis after Experimental Orchiectomy

mm to the left and right testicular sacs. Cauda
epididimis was pulled out with the testis followed
by caput epididimis. Vas deferens was ligated
along with the spermatic blood vessels. The next
step was dissection and removal of the testes.14
The incisions were then closed using silk threads
and treated with topical antibiotic (gentamycin,
Sopharma). The castrated animals were placed in
individual cages for 48-hour recovery with free
access to food and water.
SHAM ORCHIECTOMY OF MALE RATS
General anesthesia was performed with midazolam
(Dormicum, Roche) (2.5 mg/kg bdw i.p.) and fentanyl
(Fentanyl, Richter-Gedeon (0.25 μg/kg bdw i.p.).
A 10-mm-long incision was made on the scrotum
apically. The incision was extended another 5 mm
to the left and right testicular sacs. Cauda epidid-
imis was pulled out along with the testis followed
by caput epididimis. Then cauda epididimis and
the testis were returned to their normal anatomic
positions leaving the blood vessels intact. Finally
the incisions were closed using silk threads and
treated with topical antibiotic (Gentamycin, Sop-
harma). The sham operated animals were placed
in individual cages for 48 hours to recover with
free access to food and water.
During the experiment, all animals were kept
under standard laboratory conditions: air tempera-
ture 26 ± 1 °С, relative humidity 65 ± 5%, free
access to food and water. TP and oleum helianti
were injected once a week in the thigh muscle of
the animals’ hind legs.
Blood was collected after decapitation under
ether anesthesia, under a glass bell filled with
vapors of diethyl ether for 60 seconds. The blood
samples were sent immediately to the Central Clini-
cal Laboratory of Medical University - Plovdiv.
HEMATOLOGICAL PARAMETERS
Hematological parameters (complete blood count)
were determined with Coulter counter T-660. Eryth-
rocyte count, hemoglobin and hematocrit levels were
followed up. Although hematocrit is a derivative of
erythrocyte count, it was monitored for the purpose
of completeness of the survey.
STATISTICAL ANALYSIS
Statistical analyses were performed with IBM SPSS
20.0 for Windows 7. For each parameter the mean
and standard error (SEM) were calculated. The
Kolmogorov-Smirnov test was used to determine
the distribution. In normal distribution values were
compared using the Independent Samples t-test. In
non-Gaussian distribution parameters were compared
by the nonparametric two independent samples test
(Mann-Whitney U test). In all analyses, a difference
of p < 0.05 was accepted as statistically significant.
RESULTS
The results of the hematology tests are presented
in Table 3.
ERYTHROCYTES
In the acute castrated rats testosterone propionate
in a dose of 4 mg/kg bdw (p = 0.002) reduced the
erythrocyte count statistically significantly (Fig.
1). TP in the higher dose (8 mg/kg bdw) had the
same effect on erythropoiesis although it could not
reach statistical significance. Erythrocyte count was

Table 3. Erythrocytes, hemoglobin and hematocrit

Erythrocytes Hemoglobin Hematocrit

Group n
(x1012/l) (g/l) (l/l)
SOAC 10 10.14 ± 0.16 155.1 ± 2.98 0.49 ± 0.001
COAC 10 9.83 ± 0.16 156.4 ± 1.19 0.48 ± 0.01
04AC 10 8.51 ± 0.31 141.1 ± 3.94 0.397 ± 0.015
O8AC 10 9.49 ± 0.17 150.0 ± 2.39 0.45 ± 0.008
SOCHR 10 6.92 ± 0.17 145.2 ± 2.19 0.37 ± 0.004
COCHR 10 6.07 ± 0.21 139.4 ± 2.11 0.36 ± 0.01
O4CHR 10 7.62 ± 0.32 151.5 ± 1.87 0.35 ± 0.02
O8CHR 10 7.61 ± 0.06 152.7 ± 3.34 0.404 ± 0.008

Data are presented as x ± S x .

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D. Delev et al

12
◊ √∫ × Ħ

10

*† ‡Ξ SOAC

8 COAC
O4AC
O8AC
6
SOCHR
COCHR
4 04CHR
08CHR

* р = 0.02 for COAC; † р < 0.0001 for SOAC; ‡ р = 0.011 for SOAC; Ξ р = 0.013 for O4AC; √ р = 0.006 for SOCHR;
∫ р = 0.001 for O4CHR; ◊ р = 0.001 for O8CHR; Ħ р < 0.0001 for O8CHR; ◊ р = 0.01 for O8AC; × р < 0.0001 for O8AC.

Figure 1. Changes in the erythrocyte count (×1012/l).

160
∫
* †

155 Ξ◊ √

‡ SOAC
150
COAC

145
O4AC
O8AC
140 SOCHR
COCHR
135 04CHR
08CHR
130

125

* p = 0.002 for COAC; † p = 0.032 for COAC; ‡ p = 0.012 for 04AC; Ξ p < 0.0001 for COCHR; √ p = 0.004 for COCHR;
∫ p = 0.042 for COCHR; ◊ p = 0.028 for O4AC.

Figure 2. Changes in hemoglobin (g/l) – young animals.

reduced significantly in the sham operated rats by
TP in both doses (p < 0.0001, p = 0.011). The
higher dose stimulated erythropoiesis significantly
(P = 0.013).
In chronically treated animals the erythrocyte
count was significantly high (p = 0.006) in sham
operated animals in which steroidogenesis is pre-
served compared to the orchiectomised. The admin-
istration of testosterone propionate in both doses
significantly increased erythrocyte count compared
with the orchiectomised animals (p = 0.001, p <
0.0001, respectively). In sham operated rats the
difference reached statistical significance only with
the higher dose (p = 0.001) compared to treated
animals. There were no significant differences in
the examined parameter between the two doses.

Folia Medica 2013; 55(2): 51-57

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 Effect of Testosterone Propionate on Erythropoiesis after Experimental Orchiectomy

HEMOGLOBIN comparison with the two control groups (p = 0.003,

A 15-day treatment with testosterone propionate at
doses of 4 and 8 mg/kg bdw decreased hemoglobin
statistically significantly (p = 0.002, p = 0.032) in
comparison to the orchiectomised controls (Fig.
2). When compared to sham operated animals the
lower dose significantly decreased this parameter
(p = 0.012), and with the high dose there was no
significant change. There were no significant differ-
ences in the effect when comparing the two doses.
Both doses increased statistically significantly
hemoglobin in chronically treated animals compared
with the hemoglobin values in orchiectomised
animals (p < 0.0001, p = 0.004). Just like in the
acutely treated animals, here there was no signifi-
cant change in the hemoglobin values between the
groups treated with both doses.
The duration of treatment significantly increased
hemoglobin values (p = 0.028) only at a dose of
4 mg/kg bodyweight.
HEMATOCRIT
A 15-day supplementation with testosterone pro-
pionate in both tested doses decreased statistically
significantly hematocrit values compared with the
orchiectomised (p < 0.0001, p = 0.044) and the
sham operated group (p < 0.0001, p = 0.008). The
higher dose significantly increased the hematocrit
values (p = 0.006) in acutely treated animals (Fig. 3).
In the chronic experiment hematocrit increased
significantly only with the higher dose tested in
0.6
p = 0.004). Logically, testosterone propionate at a
dose of 8 mg/kg bodyweight had a statistically sig-
nificant effect on the examined parameter compared
to a dose of 4 mg/kg bodyweight (p = 0.009).
DISCUSSION
The obtained data show that after 15-day acute treat-
ment castrated male rats did not show significant
differences in the values of erythrocytes, hemoglobin,
and hematocrit compared to sham controls. This
effect is probably not due to a stimulating action
of the estrogens on erythropoiesis even though the
earlier data point at such a possibility.15 There is
quite a recent hypothesis that testosterone per se
activates erythropoiesis and there is no need to
convert it into estrogens to achieve the above ef-
fect, unlike some of its biological effects.16 The
most likely reason for the lack of statistical differ-
ence between the two controls is the short period
of monitoring. In the above-mentioned data from
clinical trials, the earliest period to monitor these
indicators is set at one month. In chronic treatment
we can observe a significant decrease in red blood
cells and hemoglobin, as well as a tendency of
hematocrit decrease.
The exact mechanism of testosterone action on
erythropoiesis is unclear. Although men and women
differ in their erythrocytes count, hemoglobin and
hematocrit values (these being higher in men) they
have comparable levels of erythropoietin and soluble

∫◊ × è
0.5
*† ‡Ξ√ SOAC
COAC
0.4
O4AC
O8AC
0.3
SOCHR
COCHR
0.2
04CHR
08CHR
0.1

* p < 0.0001 for COAC; † p < 0.0001 for SOAC; ‡ p = 0.044 for COAC; Ξ p = 0.008 for SOAC; √ p = 0.006 for O4AC;
× p= 0.03 for COCHR; Ħ p = 0.004 for SOCHR; ∫ p = 0.009 for O8CHR; ◊ p = 0.038 for O4AC; p= 0.001 for O8AC.

Figure 3. Changes in hematocrit (l/l).

Folia Medica 2013; 55(2): 51-57

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D. Delev et al
transferrin receptor (sTfR).17 On the other hand, in
the androgen-induced erythrocytosis erythropoietin
levels are low, rather than high.18 Use of androgens
in the treatment of aplastic anemia and anemia of
renal disease is effective, despite the absence of
erythropoietin stimulation.19 In a model of chronic
renal failure in rats, testosterone propionate in a
dose of 2 mg/kg bodyweight20 stimulates hemat-
opoiesis and increases the levels of hematocrit and
hemoglobin. More recent studies with follow-up of
expression of mRNA of serum erythropoietin and its
levels in orchiectomised rats or those with androgen
deficiency (induced by flutamide or cyproterone)
demonstrate that expression of EPO and its serum
levels are not altered in all three models of androgen
deprivation.21 In an experimental study in rats it
was found that the effect of erythropoietin on the
proliferation of erythroblasts is totally blocked by
flutamide (5-alpha reductase inhibitor), and partially
by cyproterone.22 It is possible that testosterone
stimulates erythropoiesis by direct affecting the
bone marrow hematopoietic stem cells. This direct
effect is mediated through the induction of insulin-
like growth factor (IGF-1) of the androgen-receptor
mediated mechanism.23 In the available literature
there is evidence that testosterone enhances the
absorption of iron, its incorporation into red blood
cells and hemoglobin synthesis.24
Anemia is partially associated with reduced
levels of circulating androgens.25 Polycythaemia
represents one of the undesirable risks of testosterone
replacement therapy which requires monitoring.26
Literature search we did of mechanism of
testosterone action on erythropoiesis explains the
observed effect of stimulation in orchiectomised rats
only at their long-term treatment. The effect was
slow, since it is receptor-mediated, and testoster-
one receptors are genetically active. Therefore, in
a 15-day application the monitored parameters of
castrated animals (despite the treatment) are more
often reduced than increased.
Of the three parameters under observation the
effect is dose-dependent only for hematocrit, where
the higher dose had a significantly stronger effect.
Since this is a leading parameter for the clinical
diagnosis of anemia, we can conclude that the effect
of testosterone on erythropoiesis in orchidectomised
rats is dose-dependent.
CONCLUSIONS
In the chronic experiment there was a significant
decrease in red blood cells and hemoglobin, and a
tendency of decrease in hematocrit after orchiectomy.
56 Unauthenticated | 203.56.241.2
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Replacement therapy with testosterone propion-
ate has a stimulating effect on erythropoiesis only
in chronic administration.
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8. Dainiak N. The role of androgens in the treatment
of anemia of chronic renal failure. Semin Nephrol
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9. Labunets IF, Butenko GM, Dragunova VA, et al. The
pineal gland’s peptides factors and the rhythms of
functions of the thymus and bone marrow in animals
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10. Bassil S, Alkaade S, Morley J. The benefits and
risks of testosterone replacement therapy: a review
Nazem, Ther Clin Risk Manag 2009;5:427-48.
11. Swerdloff R, Wang C. Three-year follow-up of
androgen treatment in hypogonadal men: pre-
liminary report with testosterone gel. Aging Male
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12. Nemeth N, Kiss F, Magyar Z, et al. Following-up
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male and female rats. Clin Hemorheol Microcirc
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13. Nemeth N, Kiss F, Hever T, Brath E, et al. Hemorhe-
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14. Zirkin B. Animal models of aging males. The Aging
Male 1998;Supp1:1-15.
15. Mirand E, Gordon A. Mechanism of estrogen action
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in erythropoiesis. Endocrinol 1965;78:325-32.
16. Faustini-Fustini M, Rochira V, Carani C. Oestrogen
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17. T’Sjoen GG, Beguin Y, Feyen E, et al. Influence of
exogenous oestrogen or (anti-) androgen administra-
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18. Dickerman RD, Pertusi R, Miller J, et al. Androgen-
induced erythrocytosis: is it erythropoietin? Am J
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19. Raich PC, Korst DR. Plasma erythropoietin levels in
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20. Ali BH, Ahmed IH. Hormonal replacement therapy
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Ren Fail 2006;28(4):331-5.
21. Voegeli TA, Kurtz A, Grimm MO, et al. Anemia
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cyproteroneacetate and orchiectomy on the erythro-
ЭФФЕКТ ТЕСТОСТЕРОН - ПРОПИОНАТА
НА ЭРИТРОПОЭЗ ПОСЛЕ ОРХИЭКТОМИИ
В ЭКСПЕРИМЕНТЕ
Д. Делев, Д. Давчева, И. Костадинов, И. Костадинова
РЕЗЮМЕ
ВВЕДЕНИЕ: Андрон-дефицитная анемия наблюдается
чаще всего при фармакогенном подавлении андроген-
синтеза или с возрастом у мужчин. Билатеральная
орхиэктомия представляет метод, применяемый
в терапии метастатической карциномы предста-
тельной железы, сопровождающейся выраженным
понижением циркулирующих сывороточных уровней
андрогенов.
Ц ЕЛЬ : Установить влияние заместительной
терапии тестостерон - пропионатом – ТП- на
некоторые гематологические показатели эритро-
поэза у мужских крыс после орхиэктомии.
Folia Medica 2013; 55(2): 51-57
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poietin system. Horm Metab Res 2005;37(2):89-93.
22. Malgor LA, Valsecia M, Vergés E, De Markowsky
EE. Blockade of the in vitro effects of testosterone
and erythropoietin on Cfu-E and Bfu-E proliferation
by pretreatment of the donor rats with cyproterone
and flutamide. Acta Physiol Pharmacol Ther Lati-
noam 1998;48(2):99-105.
23. Claustres M, Sultan C. Androgen and erythropoiesis:
evidence for an androgen receptor in erythroblasts
from human bone marrow cultures. Horm Res
1988;29:17-22.
24. Naets JP, Wittek M. The mechanism of action of
androgens on erythropoiesis. Ann NY Acad Sci
1968;149:366-76.
25. Ferrucci M, Maggio S, Bandinelli S, et al. Low tes-
tosterone levels and the risk of anemia in older men
and women. Arch Intern Med 2006;166:1380-8.
26. Rhoden EL, Morgentaler A. Risks of testosterone-
replacement therapy and recommendations for
monitoring. N Engl J Med 2004;350:482-92.
МАТЕРИАЛ И МЕТОД: Использовано 80 мужских
крыс породы Wistar, средняя масса тела – 252.3
гр. Животные разделены следующим образом: 2
контрольные орхиэктомированные, 2 симулятивно
оперированные и 4 опытные орхиэтомированные
группы. ТП применен мышечно раз в неделю в дозе
4 и 8 мг/кг массы тела; период применения – 15
дн. и 15 нед. Прослежены: число эритроцитов,
уровень гемоглобина и гематокрита.
РЕЗУЛЬТАТЫ: При хроническом опыте наблюдается
сигнификантное снижение эритроцитов и гемогло-
бина и тенденция к снижению гематокрита после
орхиэктомии. Эффект ТП на эритропоэз у крыс
с орхиэктомией дозозависима.
ЗАКЛЮЧЕНИЕ: Заместительная терапия с помо-
щью ТП в дозах 4 и 8 мг/кг оказывает стимули-
рующий эффект на эритропоэз только в случаях
продолжительного применения.
57
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