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International Journal of Basic & Applied Sciences IJBAS-IJENS Vol:16 No:05 1

160805-3737- IJBAS-IJENS @ October 2016 IJENS I J E N S

Morphological Observations on the Development of

The Mesonephros

of The Dromedary Camel Foetus Sabah. O. Elgozouli and D.I.Osman

Department of Anatomy, Faculty of Veterinary Medicine, University of Khartoum- Khartoum North -13314, Sudan.

[email protected].

Abstract-- This investigation was carried out to reveal and

evaluate the pattern of the mesonephros growth in the

dromedary camel. 30 embryos and foetuses (2 cm CVRL to 24

cm CVRL) were used to study the histology of the mesonephros.

The mesonephros of the dromedary camel foetus, consisted of

small glomeruli (primary) and two types of tubules with a set of

capillaries in between. The large glomeruli (giant glomeruli) were

observed immediately before the time of gonads differentiation to

male or female between 2 and 3 cm CVRL (71 and 74 days of

age) towards the positions where the gonads were developed.

Thus in male fetuses, the giant glomeruli surrounded the hilus at

the cranial part of the mesonephros and in this place the testes

were developed, whereas in the female foetuses the giant

glomeruli surrounded the hilus at the medial border of the

mesonephros and this the position where the developing ovaries

were observed. The large glomeruli were limited in number when

they first appeared (not more than 20) then regressed soon after

the gonads underwent differentiation, while the small

mesonephric glomeruli were observed in different stages of

development till 17 cm CVRL (112 days of age). It was clear from

these observations, that the differentiation of the gonad of the

dromedary camel foetuses could be related to the position of the

gonads in relation to the mesonephros and according to the

position where the giant glomeruli were arranged.

Index Term-- giant glomeruli mesonephros Trimester

INTRODUCTION

Regulation of mesonephric differentiation has been

studied in some mammals, such as mice (Upadhyay, Luciani

and Zamboni, 1979), sheep (Upadhyay and Zamboni, 1982),

rat and mouse (Smith and Mackay, 1991; Merchant-larios,

Moreno-mendoza and Buehr, 1993; Sainio, Hellstedt,

Kreidberg, Saxén and Sariola, 1997) and in goat (Magras,

Alifakiotis and Pampoukidou, 1997). In human (Martino and

Zamboni, 1966) and pig (Tiedemann and Egerer, 1984), the

mesonephros is well developed as excretory organ during

embryonic development. In murine species, however, the

mesonephros is primitive and non-excretory (Zamboni and

Upadhyay, 1981; Smith and MacKay, 1991). The

histogenesis and morphology of the mesonephros of the foetus

of the dromedary camel have only been briefly studied by

Musa (1982), El-Harairy, Gabr and Attia (1998), Imam (2005)

and Aly (2007).

MATERIALAND METHODS

30 embryos and foetuses were collected from Tamboul

slaughter point and from Elsalam slaughter house. The curved

crown rump length (CVRL) equation Y = 0.366X - 23.99

which was described by Elwishy, Hemeida, Omer, Mobarak

and Elsyed (1981) was used to determine the age of the

fetuses. The whole embryos and the mesonephros of the

foetuses were fixed in 10% buffered formalin. General and

special histological stains were used to investigate the

different components of the mesonephros. Small pieces of

1x1x1 mm of tissue from mesonephros were fixed in 2.5%

glutaraldehyde in 1M cacodylate buffer (Ph. 7.3), post fixed in

cold 1M phosphate buffer 2% osmium tetroxide (PH. 7.3),

then semi-thin sections 0.5 micron stained by Toluidine blue.

RESULTS

Before the time of gonads differentiation the

mesonephros presented three surfaces (dorsal, ventral and the

lateral surfaces), three borders (medial, dorso-lateral and

ventro-lateral borders) and two poles (cranial and caudal). It

resembled in outline a lemon fruit. The lateral surface was

smooth and strongly convex. The ventral and the dorsal

surfaces were slightly flattened and were joined at an angle at

the hillus ventrally. These surfaces were related to the gonads

at the hillus, to the metanephros at the dorsal surface and to

the adrenal gland cranially. The mesonephric and the

paramesonephric ducts run along the ventro-lateral border

(Fig.1).



Fig. 1. Photograph of whole dromedary camel foetus of 5 cm CVRL (79 days of age) after the removal of the viscera, showing the mesonephros (m), ovaries (long arrow),

mesonephric duct and paramesonephric duct (arrow heads).

In 2cm CVRL (71 days of age) camel foetus, the mesonphros was well developed, consisted of mesonephric corpuscles,

mesonephric tubules and mesonephric duct. The mesonephric tubules were long, numerous and coiled, had different diameter and

shapes and arranged in many rows dorsoventrally. These tubules could be differentiated into two types:

(a) Mesonephric tubules lined with single layer of low cuboidal cells with spherical central nuclei and clear lumen (b)

Mesonephric tubules lined by high cuboidal cells with big spherical nuclei and their luminal border was studded

with clearly visible microvilli, and contained material in its lumen. These tubules occupied almost the entire

mesonephros and a network of capillaries was found between these tubules (Fig.2).

Fig. 2. Photomicrograph of foetus during first trimester demonstrating mesonphric tubules lined by high cuboidal cells with pale nuclei and

many vacuoles of different sizes were scattered in the cytoplasm of the two types of mesonephric tubules but more in the tubule lined by high cuboidal cells. Note the presence of blood vessels filled with blood between the tubules. Toludine blue stain. X40.

The small glomeruli occupied the medial portion

between the mesonephric tubules and they were in the form of

masses of cells just like small nodules at the ends of the

tubules and surrounded by flat cells and had a narrow urinary

space. In 3cm CVRL (74 days of age) foetus, large glomeruli

(giant glomeruli) were observed at the ventromedial part of the

m



mesonephros . The mesonephric duct (Wolffian duct) was a

large duct and lined with cuboidal cell and situated at the

ventrolateral part of the mesonephros. The paramesonephric

duct (Müllerian duct) was small and lined with tall columnar

cells and running together with the mesonephric duct. In 4cm

CVRL (76 days of age) foetus, there was a fissure appeared

ventrally between the giant glomerular zone and the

metanephric tissue compressing the mesonephros toward the

fissure line. At this stage, the mesonephros was partially

divided into two parts, cranial and caudal. In male foetuses, a

group of mesonephric tubules in the cranial part were small in

diameter and their lining cells were changed to columnar. The

interstitial tissue between these tubules was connective tissue

rich in mesenchymal cell, fibroblasts and smooth muscle

fibres, and this cranial part of the mesonephros was the zone

where the testes would develop and suspended. The ovaries

appeared and developed at the medial part of the mesonephros

(Fig.3).

Fig. 3. Photomicrograph of some mesonephric tubules (T) in male dromedary foetus of 4cm (74 days of age) situated at the cranial pole of the mesonephros and ventral surface of the mesonephros close to the testes which grew dorsal to this zone. G: Giant glomeruli.

H&E stain. X10.

In 4.8 cm CVRL (79 days of age) female foetus, the pressure

of both the developed metanephros dorsally and the ovary

ventrally, divided the left mesonephros into small cranial and

large caudal portions. The caudal portion was more active than

the cranial one which showed signs of regression in foemale

fetuses. The right mesonephros was elongated and remained as

one unit. The small mesonephric glomeruli were demonstrated

in different stages of development and with different shapes

(“S” shape and “ɘ” comma shape). Glomeruli with and

without blood entrance were surrounded by glomerular

capsule which was lined by simple squamous cells at the

parietal layer and podocytes and capillary plexus at its visceral

layer with narrow urinary space

T

G



Fig.4: Photomicrograph of small mesonephric glomeruli at different stages of development in “S” shape, “ɘ” comma shape, glomeruli with blood vessels entrance (V) and without blood vessels entrance, from foetus during first trimester.

Toludine blue stain X 40.

The large glomeruli (Giant glomeruli) were grouped at

the medial portion of the mesonephros and surrounded the

hilus close to the ovaries in female foetues, while the Giant

glomeruli in male foetus, were concentrated in the cranial part

of the mesonephros close to the testes. The large glomeruli

were lined with two types of cells: squamous cells and high

squamous or dome shape cells in the parietal layer of

glomerular capsule with wide urinary space. The blood

vessels of the giant glomeruli were in the form of tuft of

sinuses (Fig.5).

Fig. 5. Photomicrograph of mesonephroic large (Giant) glomeruli from foetus of 17cm CVRL(112 days of age) lined with squamous cells (s) and

high squamous (dome shape) cells (d) in the parietal layer of glomerular capsule, had a wide urinary space and the blood vessel in the form of tuft

of sinuses. P: Podocytes cells. Toludine blue stain. X100 .

Haemopoitic cells in different stages of development

and numerous primordial germ cells were observed in the

parenchyma of the giant glomeruli and in the small glomruli.

Large podocytes lined the visceral capsular layer of Bowman

of the mesonephric giant glomeruli.

In 6 cm CVRL (82 days of age) male foetus , the

testis was observed as small mass suspended by the

mesogonadal ligament to the cranial pole of the mesonphros

and connected to the zone of the developed efferent ductules.

Almost all the giant glomeruli in male foetuses were

accumulated at the cranial part of the mesonephros toward the

testes. Some mesonphric tubules and some giant glomeruli

situated beneath the testes adhered with the testes and became

regular tubules lined with cuboidal cells (Fig.6).

v

s

ɘ

d

s

P



Fig. 6.A. Photomicrograph of a male foetus of 6 cm CVRL (82days of age), demonstrating the testes (T) suspended by the mesogonadal ligament to the cranial pole of the mesonphros (m) and connected to the zone of the developed efferent ductules. mt: metanephros . H&E stain. X4.

Fig. 6.B. Photograph of ventral view at the lumber region of dromedary camel male foetus of 14.5cm (105 days of age), demonstrating the testes (t) suspended to the mesonephros (m) at the cranial pole and attached to the metanephros (mt) obliquely.

In 7, 8 and 8.5 cm CVRL (85, 87and 89 days of age)

female foetuses, the caudal portion of the mesonephros was

well developed to become double the size of the metanephros

and it surrounded the metanephros ventrally in a spindle

shape. The cranial portion disappeared in the left

mesonephros of female foetuses, and retained as efferent

ductules in male foetuses. The Müllerian duct changed its

lining epithelium from tall columnar to pseudostraified cells in

female foetuses. Some signs of regression appeared during

these stages gradually in small parts of the mesonephros. The

first signs appeared in the capillaries in between the

mesonephric tubules which were invaded by large pale cells

with big dark nuclei. Then the lumen of the mesonephric

tubules was filled with material and sloughed and damaged

lining epithelial cells and plasma cell were observed scattered

between the lining epithelial cells. These signs of degeneration

were not observed in all tubules in the same time, but they

started in the cranial and lateral tubules of the left

mesonephros earlier than the right one in the female foetuses

and in the giant glomeruli more earlier than in the small

glomeruli. In 11 cm CVRL (96 days of age) foetus, the caudal

portion of the mesonephros regressed to half the size of the

metanephros. The left mesonphros was situated at the ventral

caudal portion of the metanephros, whereas the right one was

still in large size and elongated and it surrounded the caudal

half of the metanephros ventrolaterally. The mesonephric

A

B

t t

m

mt

mt

mt

m

T

A



capsule was in the form of dense connective tissue. New

generations of small glomeruli were observed in different

stages of development. The giant glomeruli were accumulated

at the hilus region in the left mesonephros and scattered along

the length of the right mesonephros in female foetuses and

connected to the ovary and the metanephros by a mesogonadal

ligament which was rich in blood supply (Fig. 7).

Fig. 7.a. Photomicrograph from a female foetus of 11 cm CVRL (96 days of age), illustrating giant glomeruli (g) situated at the hilus of the left

mesonephros connected to the ovary (o) and the metanephros by connective tissue rich in blood supply. The ovary at this stage was situated

above and cranial to and in contact to the left mesonephros. Müllerian duct (arrow). H&E stain. X4.

Fig. 7.b. Photograph of a ventral view of a female foetus of 11 cm (96 days of age), showing the ovary (o), mesonephros (m), metanephros (mt)

at different levels (the right metanephros was more cranial),the mesonephric duct (arrow) and the paramesonephric duct (arrow heads).

The ovaries at this stage were situated above and cranial to the

mesoneohros. The left ovary was large in size and in contact

with the left mesonephros, while the right ovary was small and

had no direct contact with the right mesonephros (Fig.7). The

Müllerian duct merged with the caudal pole of the developing

left ovary. Hematopoietic stem cells, blood cells,

macrophages, primordial germ cells, B and T lymphocytes

were seen within the giant glomeruli. Part of the right

mesonephros was in close contact with the right metanephros

and connective tissue with fine reticular fibres connected the

right metanephros with the right mesonephros. There was a

large space between the left metanephros and the left

mesoneohros. In 13 cm CVRL (101days of age) female

fetuses, the mesonphros parenchyma increased in cell

components mainly fibroblasts and smooth muscle fibres. The

giant glomeruli collapsed and the orifices of the mesonephric

ducts decreased in their calipers. At this stage, the cranial part

of the left mesonphros was connected to the ovary by

mesovarin, and this part of the mesoovarian enlarged cranially

and became as rosy funnel above the cranial pole of the left

mesonephros. Many small rounded tubules were lined with

simple cuboidal cells and some mesoneohric tubules were

filled with pink material at the cranial part of the

mesonephros. The mesonephros cell components in the matrix

increased especially at its lateral aspect which included the

paramesonephric duct. The paramesonephric ducts increased

in size in female foetuses. Long microvilli, pale nuclei, many

vacuoles of different sizes were found in the tubules which

were lined with low cuboidal and tubules lined with high

cuboidal epithelium but more in the tubules which were lined

by high cuboidal cells. In 15 cm CVRL (106 days of age), the

cranial part of the mesonephros was separated from the ovary

and became narrow and long, and its end was funnel shaped

and faced the ovary and lined with pseudostratified epithelium

(Fig.8)

a b

m m

mt mt

o o

o mesonephros

metanephro

s

g



Photomicrograph from 15 cm CVRL (106 days of age) female foetuses, the cranial part of the left mesonphros was separated from the ovary and became narrow

and long, its end was funnel shaped, lined with pseudostratified epithelium and faced the ovary (arrow).

H&E stain. X4.

In 22 cm CVRL (126 days of age) foetus, the

mesonephros was completely collapsed in female foetus and

became as small spherical mass of dense connective tissue. In

male fetuses the mesonephros were regress and collapsed

during the second trimester

DISCUSSION The mesonephros of the dromedary camel foetus was

observed histologically at 0.9 cm CVRL as a narrow strip

along the roof of the thoracolumber region of the vertebral

column Aly (2007). Osman, Farouk, Eidaroos and Ahmed

(2008) observed it in the same region at 0.5 cm CVRL in the

dromedary camel. Several authors described the mammalian

mesonephrosi as mesonephric nephrons consisted of a

glomerulus-like body, a proximal tubule and a distal tubule

(Martino and Zamboni, 1966; Schiller and Tiedemann, 1981;

Tiedemann and Egerer, 1984; Smith and MacKay, 1991). In

the present study, the mesonephros of the dromedary camel

foetuses consisted of primary small glomeruli, secondary large

glomeruli (Giant glomeruli) and two types of tubules: 1-

Tubules lined with single layer of low cuboidal cells with

spherical central nuclei and clear lumen. 2-Tubules lined by

highly cuboidal cells with big spherical nuclei and their

luminal surface was studded with microvilli. In the dromedary

camel, these two types of mesonephric tubules were described

by Bareedy, Anis, Abbas, Ewais, and Amar (1982), Emara

(1989) and Aly (2007). Such morphology of mesonephric

tubules was also demonstrated in buffalo foetuses (Moustafa,

Enany, Osman and Amin,1986) and in human foetuses

(Sadler, 1995). In the present observations, the mesonephric

tubules of the dromedary camel foetus were oriented

dorsoventrally, similar to the observations of Upadhyay,

Luciani and Zamboni (1979) in the mouse foetuses. Upadhyay

and Zamboni (1982) described very large glomeruli occupied

the proximal third of sheep mesonephros and, according to its

size, was referred to as “giant glomeruli” as described by

Bremer (1916) and Davies and Davies (1950). Smith and

Mackay (1991) stated that, glomerulus-like structures were

found at some stages of development and consisted of

capillaries opposed to the ventral aspects of the tubules in

mouse foetuses. The S-shaped glomeruli in either degenerated

or remained as tubules were observed in mouse foetuses. In

the present findings in the dromedary camel fetuses, the large

glomeruli were limited in number (not more than 20) and

regressed when the gonads were differentiated, but new

generations of small mesonephric glomeruli in different stages

of development (“S” shape, “ɘ” comma shape and other

stages) remained till 17 cm CVRL (112 days of of age). This

observation may suggest a relation between the giant

glomeruli and the gonad differentiation or between the small

glomeruli and the developing metanephros.

The present observation may support the

suggestion of Ward, Cornillie, Erkens, Loo, Casteleyn,

Poucke, Burvenich, Hoorebeke, Ginneken, Peelman, and

Broeck (2010) who believe that the mesonephric glomeruli

continue to grow in porcine foetuses, even when the cranial

part of the mesonephros started to regress. These authors did

not mention whether these glomeruli were giant or small

glomeruli. This phenomenon may be explained by the fact that

the growing foetus requires a sufficiently large glomerular

filtration surface provided by small or large glomeruli. During

the development of the metanephros, the mesonephros of

porcine foetus continued to maintain its excretory function as

reported by Patten (1948). The giant glomerulus, which begins

at the first month of gestation in sheep foetuses, was

characterized by hypercellularity, thickening and obliteration

of the capillaries, and loss of Bowman’s capsule on the ventral

metanephros

mesonephros

ovary



aspect of the glomerulus (Upadhyay and Zamboni,1982). In

the present study, the giant glomeruli had complete parietal

and visceral layers of Bowman’s capsule and the capillaries

were in the form of sinuses. Magras, Alifakiotis and

Pampoukidou (1997) reported that the existence of giant

glomeruli, a peculiar structure located dorsal to the genital

ridge in the cranial part of the mesonephros of the goat, must

play an important role in the gonadal development because

epithelial cells from mesonephric tubules and from the giant

glomeruli invaded the gonads. Upadhyay and Zamboni (1982)

observed an active mobilization of glomerular cells egress

from the giant glomerulus passing through the interruptions of

the Bowman’s capsule on its ventral aspect to the ovary and

testis in association with the germinal cells in sheep foetuses.

In the present study, the accumaltion of the large glomeruli

were connected to the gonads by dense connective tissue rich

in blood supply (mesogonadal ligament).

In the present investigation, the large

glomeruli (giant glomeruli) were observed near the gonads,

between 2and 3 cm CVRL (74 and 76 days of age) before the

time of gonads differentiation to male or female foetuses. The

giant glomeruli in male fetuses were surrounded the cranial

part of the mesonephros, while in the female foetuses were

near the hilus. It was clear from these observations that the

differentiation of the gonads of the dromedary camel foetuses

could be related according to the position of the gonads in

relation to the mesonephros and according to the position

where the giant glomeruli were arranged. In the present study,

the cranial part of the mesonephros had different way of

development and fate between male and female foetues. In

male fetuses, the cranial part of the mesonephros did not

separate from the mesonephros but it was transformed into

ductuli efferentes first, then other tubules and some giant

glomeruli contributed in the formation of the epididymis later.

The cranial part of the mesonephros in female foetues was

divided, and when the ovaries were developed this part

regressed and disappeared.

Sainio, Hellstedt, Kreidberg, Saxén and

Sariola (1997) reported that, in mice and rat, the cranial part of

the mesonephros was derived from the Wolffian duct and the

caudal tubules were derived from the mesonephric

mesenchyme. Consequently, it's possible to believe that the

hormone-dependence of mesonephros was only functioning in

the cranial part of mesonephric tubules of male foetuses after

the appearance of testes and release of its hormones. On the

other hand, the cranial part of the mesonephros disappeared in

female foetues and its may be due to anti hormones as it was

explained by the above authors and observed in the present

study.

In male foetuses of the dromedary camel

between 3 and 4 cm CVRL (74 and 76 days of age), in the

present investigation, the primitive ductuli efferentes were

observed in the cranial part of the mesonephros, the place

where the testes would develop and suspended by a short

mesogonadal ligament attached to the dorsal surface of the

mesonephros. The attachment between the mesonephros and

the developed testes contributed and required for the next step

of other mesonephric tubules transformation, Merchant-larios,

Moreno-mendoza' and Buehr (1993) explained this relation

between the mesonephros and testes. The differentiation of

Sertoli cells and Leydig cells proceeds in the absence of

mesonephros at early stages of development but endothelial

cells and peritubular myoid-like cells migrated into the

gonads, so they suggested that these cells might be

mesonephric cells required for seminiferous cord formation. In

the present observation, in female foetuses during the age

between 3 and 4 cm CVRL (74 and 76 days of age), the

ovaries were situated in the middle part of the medial border

of the mesonephros and connected to the hilus. Zolain (2011)

stated that in 22 cm CVRL (126 days of age) dromedary camel

foetus, the regressing mesonephros disappeared completely on

the left side, while in the right side it appeared like a small

prominence in the caudal pole of the right metanephros and

the left ovary differentiated earlier than the right one and was

separated from the mesonephros. This finding was in

agreement with the present finding and this result may explain

the increasing incidence of pregnancy in the left horn in adult

camels than the right one and that the left ovary may be more

active than the right ovary. The left mesonephros in female

foetuses was divided into cranial and caudal parts before the

right one and this is in coordination with the advanced ovarian

growth rate.

In dromedary camel foetus, Osman, Farouk,

Eidaroos and Ahmed (2008) reported that the mesonephros

began its regression from 3.7 cm CVRL. The regression

comprised apoptotic changes among the tubular and

glomerular elements of the mesonephros. However, Bareedy

(1982) stated that the mesonephros of dromedary camel

gradually degenerates from 5 cm CVRL, while Emara (1989)

reported that the mesonephric degeneration occurred at 3.8 cm

CVRL and El-Harairy, Gaber and Attia (1998) noticed that the

mesonephros started to degenerate at 15 cm CVRL, while, Aly

(2007) observed the degeneration at 4.7 mm CVRL.

The result of this study demonstrated that,

the signs of regression of the mesonephros were demonstrated

in female foetuses earlier than in male fetuses and the

regression signs began by large pale cells invaded the

capillaries between the mesonphric tubules in 7 cm CVRL(85

days of age). The giant glomeruli showed signs of regression

and degeneration after the gonads were differentiate in male

and female foetuses, whereas new generation of small

glomeruli were developed till the end of the first trimester in

male foetuses. The mesonephros regressed and disappeared

during the first trimester in female foetuses, whereas in male

foetuses it disappeared during the second trimester.

CONCLUSION

Mesonephros could be used as a guide in the gonads

differentiation to ovaries or testes before or at 3 cm CVRL (74

days of age) of dromedary camel foetus, grossly according to

the position of the gonads in relation to the mesonephros and

histological according to the position where the giant

glomeruli of the mesonephros were arranged.



ACKNOWLEDGMENT

This work was carried out at the Department of

Anatomy Faculty of Veterinary Medicine, University of

Khartoum-Sudan, with financial support from the German

Academic Exchange Serves (DAAD).

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