2023.08.04.19
Files > Volume 8 > Vol 8 no 4 2023

The histomorphological appearance of the testes in Alloxan-induced
diabetic rabbits

Hasanain
Emran 1*, Khyreia Habeeb 2, Abeer
Majeed 1
1 Departments of Veterinary Surgery and Obstetrics, College of
Veterinary Medicine/ University of Baghdad. Baghdad, Iraq; [email protected].
2 Departments of Anatomy and Histology, College of Veterinary
Medicine/ University of Baghdad. Baghdad, Iraq; [email protected].
1 Departments of Veterinary Surgery
and Obstetrics College of Veterinary Medicine/University
of Baghdad. Baghdad, Iraq; [email protected].
* Corresponding author:
E-mail: [email protected].
Available from. http://dx.doi.org/10.21931/RB/2023.08.04.19
ABSTRACT
This study assessed the histomorphological changes in testicular tissues due
to the experimental diabetes
mellitus (DM) generated in rabbits with Alloxan. Twenty-four adult male rabbits
were used and allocated randomly into two equal groups (n=12 of each). The first
group served as a control group and received normal saline only. The second
group (diabetic group) was injected with Alloxan at a 100mg/kg IP dose. The
serum glucose level was estimated at (0 min), 3 days and then (1,2 and 3 months),
by aspiration of a blood sample from the jugular vein mixed with anticoagulant (EDTA)
to obtain serum. The testosterone hormone was assayed from the serum obtained
by centrifugation of blood samples using a special kit. Testicular biopsies
were harvested through surgical castration at (1,2, and 3 months)
post-administration of Alloxan. Results displayed a marked increase in glucose
levels in the diabetic group starting from day three till the end of the experiment,
with high differences between the two groups.
Moreover, testosterone levels significantly
decreased in the diabetic group compared to the control group. Our histomorphological
examination confirmed that Alloxan leads to testicular damage in rabbits,
represented by testicular
atrophy, necrosis focusing in spermatogenic cells and separation of germinal
epithelium. In conclusion, the injection of Alloxan succeeded in inducing
(DM) with clear alteration in studied parameters.
.
Key Words: Biochemical, Testicular Parameters, Alloxan, Rabbits.
INTRODUCTION
Diabetes Mellitus (DM) is a prevalent chronic
metabolic disorder. It is considered one of the significant diseases
of our time and should not be neglected due to damage and dysfunction in multiple
organ systems. It is now the seventh greatest killer of humankind
due to its high prevalence and mortality1. DM is broadly classified under two
major categories, which include insulin-dependent
DM (type I) due to loss or destruction of
β-Langerhans islet cells of the pancreas, which leads to an absolute lack of insulin; this type affects children
and young adults and
non-insulin-dependent (DM) (type 2) in the adult in which β cells retain some functional
ability2. DM is characterized by increased blood sugar levels
(hyperglycemia), glycosuria,
polyuria, polyphagia, polydipsia, and abnormal lipid and protein metabolism3,4.
Furthermore, DM is mostly accompanied by severe complications such as macro-vascular diseases, mainly
myocardial infarction, congestive cardiac failure, and arteriosclerosis5, and micro-vascular complications include
diabetic neuropathy, diabetic nephropathy, and diabetic retinopathy6. Moreover, several studies indicated that DM has a detrimental effect on male sexual and reproductive
functions as it lowers gonadotropins and
testosterone hormones (responsible for spermatogenesis), resulting in decreased libido,
delayed sexual maturation, and infertility with poor semen quality considering the central role of the
testis represented by the production of testosterone and sperm which work to
retain the characteristics of male and species preservation 7,8,9.
Experimental induction of
DM can be achieved surgically through total or partial pancreatectomy10. The pharmacological induction of DM
can
be achieved by injecting chemical
agents such as Alloxan and Streptozotocin, which are most commonly used to cause damage to β cells of the pancreas as
their diabetogenic dose is usually 4 to 5 times less than their lethal dose. The
dose of these agents varies among the animal species, age, and nutritional
status. It can be administered IV, IP, or SC. 11. The present study aimed to assess the histomorphological
changes in testicular tissues in diabetic rabbits to identify potential factors that will help design more
targeted experiments.
MATERIALS AND METHODS
Experimental animals
The current study was conducted on (24) normoglycemic local strain male rabbits, with
an average age ranging from 12-16
months and initial weight ranging from 2000g to 2500g. The rabbits were
obtained from the animal house of the faculty of Veterinary
Medicine/University of Baghdad.
Management of the animals
The rabbits were kept in individual standard cages under the same
managerial and hygienic conditions for three weeks before diabetes induction in
the animal's house at the College of Veterinary Medicine/ University of Baghdad
to become familiar with their new home and to monitor any possible
abnormalities that may have happened. The cages were floored with a
layer of sawdust for rabbits' urine absorption due to excess urination of rabbits
after Alloxan injection. Rabbits were maintained under well-ventilated
conditions with 14 hrs. light/ day, controlled temperature (23-25Co),
and humidity (40- 45). They were fed standard pellets and greens feed (3 times
a day) and were offered to tap water ad libtum throughout the experimental period. During quarantine, rabbits were
screened and dewormed with a prophylactic anthelminthic drug (Ivomec1%, 0.2 mg/kg
SC; India) against endo and ectoparasites. All works were conducted at the same
time in the morning to avoid the effect of daily rhythm on the study results. One day before study initiation, rabbits
were weighed using an electronic balance scale (China). The experimental
protocols used in the current study were approved by the Institutional Animal
Ethics Committee, Faculty of Veterinary Sciences and Animal Husbandry, and
conform to the guidelines for the Care and Use of Laboratory Animals for
Research. The duration of the experiment was set at three months.
Induction of Diabetes Mellitus
Rabbits
(n=24) were used, and they fasted
overnight before Alloxan administration; water was not withdrawn before
injection of Alloxan. The ventral lateral abdominal area (lateral to the
umbilicus) was prepared aseptically before injection under mild sedation
(Xylazine hydrochloride 2%, 3 mg/kg BW IM; Spain). 12. A fresh solution of Alloxan monohydrate (Sigma,
Germany) was prepared by dissolving it in
0.9% NaCl saline in a concentration of 10% and used immediately (since it is
known to be very unstable). The rabbits were randomly and equally divided into
two groups. The first group (n=12) was a standard control group, injected with only
normal saline (IP) as
a vehicle in a 1ml/kg BW dose. The second
group (n=12) served as the Alloxaned diabetic group, in which diabetes was induced
by injection of 100 mg/kg BW, Alloxan (IP) after dissolved in isotonic solution13, and the research was focused on this group. Before giving Alloxan,
the average blood glucose levels of all rabbits were estimated. Immediately
after two hours from alloxan administration, rabbits were given 20 ml of 5%
glucose solution to counteract the early phase of drug-induced hypoglycemia
shock. The blood glucose levels were measured three days post-Alloxan
administration using a manual glucometer
(Accu-Chech
Active, Roche Diagnostics, Germany). Rabbits with
blood glucose more than 200 mg/dl were declared
diabetic and were selected for the study.
Study
parameters
For estimation of glucose levels, three milliliters of blood samples were drawn from each rabbit through jugular vein puncture under aseptic condition at zero time ((base
data) and then (3 days, one, two, and three months)
post-Alloxan injection for control and diabetic groups. The samples were put into labeled
centrifuge tubes containing anticoagulant
Ethylene-Diamine-Tetra-Acetic acid (EDTA), then centrifuged at 4000 revolutions per
minute for 10 minutes to recover blood serum and stored under refrigerated
condition before glucose analysis was carried out. The glucose values were recorded immediately as mg/dl.
The testosterone assay (ng/ml) was
performed by collecting venous blood samples from all rabbits in the morning before access to feed and water. Sera were
removed by centrifuging blood at 4000 revolutions per minute for 10 minutes and
then stored at -20 C° until assayed. The serum testosterone hormone concentration
was measured by radioimmunoassay (RIA) using commercial kits obtained
from (Diagnostic Systems Laboratories Inc. Texas, USA). This hormone was
measured before Alloxan injection (zero time) and
then (one, two, and three months) post-Alloxan injection for control and
diabetic groups.
Histopathological assessments of testes
All rabbits were subjected to surgical castration (orchidectomy)
under the effect of mild general anesthesia represented by Medetomidine
(1mg/kg) and Ketamine (100 mg/ml) combination in a dose of 0.25 mg/kg and 30
mg/kg, respectively and administered IM14,15. Testicular
tissue biopsies were examined
monthly (for three months) (12 bucks/group) and (4 bucks/period). The biopsies were harvested and carefully trimmed to a suitable size (1cm3),
fixed in bouin solution for 24 hrs. The
samples were labeled and washed in running tap water before processing and then transferred to a graded series of ethanol (70%, 80%, 90%, and 100%), cleared in xylene. The tissues were infiltrated in molten paraffin wax in an oven at
58°C., after which the tissues were embedded in wax and blocked out. The paraffin-embedded biopsies were sectioned at 5μm thickness using a rotatory microtome (Semi-automated Rotary Microtome
Wetzlar, Germany). The histological section was stained with Hematoxylin and Eosin (H & E)16 and observed thoroughly
under a light microscope equipped with a
camera (Olympus, Tokyo, Japan).
Statistical Analysis
All data generated were reported as (Mean ± SEM). In addition, Way Analysis of Variance (ANOVA) was
used to test differences between the two groups, followed by Duncan's Multiple
Range test. The significance level was set at P<0.0517.
RESULTS
Clinical signs
Three days post-Alloxan injection, there
were clear signs of hyperglycemia as observed in the diabetic rabbit's group, represented
by frequent urination, excessive thirst, decreased physical activity, and a
tendency to lie down compared to the control rabbits group, reflecting standard
behavioral patterns.
Estimation of serum glucose concentration
In Alloxan-induced diabetic rabbits,
glucose concentration increased steadily (P<0.05) up to three months with the highest value (314±15.33 mg/dl) at this
time compared to control group rabbits, which remained relatively stable
(standard level) during all periods of observations at about (95 and102 mg/dl).
Generally speaking, there were significant differences (P<0.05) between both
groups starting from day three and forward periods (Figure 1).

Figure
1. Mean serum glucose values (mg/dl) in two groups at different intervals. No.=12
rabbits/group. Means with different vertical superscripts represent significant
differences at (P<0.05) between the
control and diabetic groups.
Serum
testosterone assay
The
testosterone values showed no significant (P> 0.05) difference between
the control and diabetic groups at zero time. In contrast, testosterone levels decreased
remarkably (p<0.05)
in the diabetic rabbits group with the advancement of experimental time. It was
recorded (0.09±0.00ng/ml) at the end of the experiment compared
to the control group (0.67±0.15ng/ml) (Figure 2).

Figure
2. Mean testosterone values (ng/ml) in two groups at different intervals.
No.=12 rabbits/group. Means with different vertical superscripts represent a
significant difference (P<0.05) between
the control and diabetic groups.
Histopathological findings
Control group
Photomicrographs in control testes depict normal histo-architecture
of the testes, which expresses Seminiferous Tubule (ST), which had a definite
tubular basement membrane and lined by germ cells epithelium containing different types of germ cells; Spermatogonia lying on
the basement membrane beneath it is the supporting Sertoli cells. The interstitial tissues found between ST contain
interstitial cells or Leydig cells (Figure 3).

Figure 3. Histology
in the testis of the control group shows ST
lined by a basement membrane (blue arrow) containing spermatogonia (gray arrow)
and Sertoli cells (black arrow), different stages of spermatozoa in the lumen
(star) and interstitial tissue between the tubules containing Leydig cells
(green arrow) (H&E; X400).
Diabetic group
Photomicrograph of the testis, one-month post-injection of Alloxan,
showed
atrophy of ST, which contains degenerated germ cells,
thrombosis of tunica vasculosa with fibrosis of tunica albuginea and
intertubular tissue (Figure 4). At two months, the testicular section revealed a decrease in epithelial cells of the ST and vacuolation of Sertoli
cells (Figure 5). In another section, there was vacuolar degeneration of spermatogonia with the formation
of intratubular multinucleated spermatid giant cells (Figure 6). At the end of the experiment (three months), the testicular section
displayed necrosis of all ST with mononuclear
cell infiltration around the remnant tubules (Figure 7), in
addition to the configuration of ST, which devoided sperms, destruction, and sloughing of the
basement membrane (Figure 8).

Figure 4.
Photomicrograph in the testis of the diabetic group, one-month
post-injection of Alloxan, show atrophy of ST, which contain degenerated germ cells (black arrow), thrombosis of tunica
vasculosa (blue arrow) with fibrosis of tunica albuginea (green arrow) and
intertubular tissue (red arrow) (H&E; X400).

Figure 5.
Photomicrographs in the testis of the diabetic group, two months
post-injection of Alloxan, show a
decrease in epithelial cells of the ST (blue arrows) and vacuolation of Sertoli
cells (black arrows). (H&E; X400).

Figure 6.
Photomicrograph in the testis of the diabetic group, two months
post-injection of Alloxan, show
vacuolar degeneration of spermatogonia (black arrows) with formation of
intratubular multinucleated spermatid giant cell (blue arrow). (H&E; X400).

Figure 7. Photomicrographs in the testis of the diabetic group, three months
post-injection of Alloxan, show necrosis of all ST (black arrows)
with mononuclear cell infiltration around the remnant ST (blue arrow).
(H&E; X400).

Figure 8. Photomicrograph in the testis of the diabetic group, three-month
post-injection of Alloxan, shows the configuration of ST, which devoided
sperms (black arrow), destruction and sloughing of the basement membrane (blue
arrow) (H&E; X400).
DISCUSSION
The results of the present study declared that IP injection of a
single dose of Alloxan induced a model of DM in rabbits. After three days, the
hallmark feature was persistent hyperglycemia, which was monitored throughout
the experiment in the diabetic group. These might be attributed to the specific,
irreversible cytotoxic effect of Alloxan, which rapidly damages the β cells of
the islets of Langerhans in the pancreas and subsequently results in a sharp reduction
of insulin secretion from these cells and impairment of glucose uptake by
muscle and fat cells, this interpretation was support by18 who reported that apparent increase in glucose level in Alloxan-induced
diabetic rabbits was attributed to marked damage to β cells and reducing
insulin secretion resulting in hyperglycemia. On the other hand, previous study
19 suggested that Alloxan and its metabolites tend to concentrate in
pancreatic islet tissue relative to some other tissue. The harmful effects of Alloxan,
causing hyperglycemia, might be due to rapid inhibition of the insulin
secretory mechanism.
Furthermore, 20 observed that
glucose formation is promoted in insulin deficiency, partly due to increased
conversion of glycogen to glucose but mainly by gluconeogenesis. Similarly, in an
experimental trial in mice, Syiem reported that Alloxan is the most prominent
diabetogenic chemical used in diabetes research21. It is a cytotoxic glucose analogue causing selective destruction
of β-cells in the pancreas through the generation of reactive oxygen system
(ROS), which causes severe anemia responsible for hyperglycemia and many other complications.
The clinical signs of hyperglycemia, as observed in studied
rabbits, were constant with that noticed by 22 when they induced diabetes in the dog at the same dose of Alloxan
used in our study, which included polyuria, polyphagia, glycosuria,
in-appetence, general weakness, depression and recumbency. Likewise, 23 recorded polydipsia, polyuria, and polyphagia in diabetic rats.
In the present work, it is noteworthy herein to mention that serum
testosterone level was remarkably decreased in the diabetic group, which is one
of the indicators of dysfunction in testicular androgen metabolism; this may be
due to the diminished number of Leydig cells, which are responsible for the
secretion of this hormone, evoked from the harmful effect of DM. This
interpretation is fundamentally consistent with a previous study by 24 who noticed a decrease in testicular testosterone, which is
associated with histological alterations in androgen target cells, i.e., Leydig
cells. In an experimental trial, 25 have
reported that hyperglycemia causes dysfunction of Leydig cells. Thus, these
cells cannot secrete testosterone, which can cause a reduction of serum levels of
this main androgenic hormone level in streptozotocin-induced diabetes in male
rats.
The testis is a vital organ in the male
reproductive system and is well vascularized; it is located in an "out-pocketing"
of the abdominal cavity called the scrotum. Testes have dual functions, i.e.,
exocrine (spermatogenesis) and endocrine (synthesis of male hormones, mainly testosterone). Histologically, the testes are enclosed in a testicular
tissue capsule through which blood vessels and nerves arrive and depart from
the organ. The testes comprise three layers: tunica albuginea, tunica
vaginalis, and tunica vasculosa26.
The histological section of the normal testis in the present
investigation showed cells, including spermatogonia and Sertoli cells, which
were seen laying on the basement membrane of ST in addition to different stages
of spermatozoa. The Leydig cells were present in between the tubules.
In our study, the diabetic group reflected atrophy of ST with
aggregations of tissue debris representing dead germ cells in their lumen. Furthermore,
vacuolation of Sertoli cells is a common feature of morphological injury of
Sertoli cells and often accompanies generalized germinal cell
degeneration/atrophy. This was indicative of the harmful effect of Alloxan. The
present findings were in agreement with a study in rat27.
Moreover,
we noticed multi-core giant cells in the ST. Similarly, Cernochova and Kamarad
observed multinucleated giant cells in some ST. At the same time, these cells
were found in systemic, toxic, infectious, ischemic pathologies and in
cryptorchidism, causing tubular atrophy28.
Other histopathological sections in the current study in the diabetic
group revealed an irregular shape of ST, which was devoid of germ cells, absence
of Leydig cells, which was replaced by fibrous connective tissue containing mononuclear
cells infiltration in addition to increased sloughing of germinal
epithelium. This may be due to a lack of testosterone, which responds to the spermatogenesis
process and finally causes histopathological damage in the testis. Monsees
suggested that the decreased testosterone reflected on Sertoli cells function leads
to loss of germ cells, loss of contact between them, reduction of the thickness
of the seminiferous epithelium, and finally, destruction of testicular tissue29.
Moreover, it was speculated that the pathological changes of seminiferous
epithelium may disrupt the Sertoli and germ cells and, therefore, spermatogenesis
and may also lead to germ cell loss30. Elshennawy and Abo Elwafa 31
reported that spermatogonia are highly sensitive to toxicants because of their
mitotic activity.
Moreover, the defects of spermatogonia will affect the development
of the stages of spermatogenesis. Also, the present results declared that ST has
various degrees of degeneration of spermatogonia with numerous apoptotic cells.
These findings are in agreement with that were reported by Al‑Damegh32.
CONCLUSION
In conclusion,
the results of the current study reveal that DM in rabbits was successfully
induced with a single dose of Alloxan via the IP route. It caused a marked
elevation in serum glucose levels and a severely diminution of testosterone
values. Furthermore, DM alters
histomorphological parameters of testicles like testicular atrophy and
degenerative changes in the testicles, which were prominent especially at the end of the experiment in the diabetic
group compared to the control group and
reduces sperm production in an animal model.
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Received: 28 September 2023/ Accepted: 15 November 2023 /
Published:15 December 2023
Citation: Emran H, Habeeb
K, Majeed A.The histomorphological appearance of the testes in Alloxan-induced
diabetic rabbits. Revis Bionatura 2023;8 (4) 19. http://dx.doi.org/10.21931/RB/2023.08.03.19