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Revista mexicana de ciencias pecuarias

versión On-line ISSN 2448-6698versión impresa ISSN 2007-1124

Rev. mex. de cienc. pecuarias vol.7 no.1 Mérida ene./mar. 2016

 

Articles

Morphometric study of the epididymes during the postnatal development in Barbados Blackbelly ram lambs

Anahy Danae Vargas-Velázqueza 

Héctor Jiménez-Severianob  * 

a Licenciatura en Medicina Veterinaria y Zootecnia, Universidad Autónoma Metropolitana, Xochimilco, DF, México.

b Centro Nacional de Investigación Disciplinaria en Fisiología y Mejoramiento Animal, INIFAP, Ajuchitlán, Querétaro, México.


Abstract:

To characterize the development of the epididymides, Barbados Blackbelly ram lambs were castrated at birth and every three weeks until wk 21 (n=4 to 6 per group). The individual epididymal weight was recorded; the three anatomical regions (caput, corpus and cauda) of the left epididymis were weighed, and samples taken for morphometric studies. The percentage of tubular tissue was calculated, as well as the tubular diameter, the width and area of the muscular layer, the height and area of the epithelium, and the diameter and area of the tubular lumen. Data were analyzed to determine differences among the anatomical regions and ages. The greatest growth of the whole organ was observed between 9 and 18 wk; the cauda started developing earlier than the other anatomical regions; the cauda was heaviest between birth and wk 12, but from 15 to 21 wk the caput and cauda weights were similar to each other. Overall, tubular diameter, width and area of the muscular layer, and luminal diameter and area were greatest in the cauda epididymidis. The epithelium height was greatest in the cauda until wk 9, but the situation reversed from wk 12 onwards. According to previous information for this breed, cauda started developing before the increase of circulating testosterone concentrations, and before the seminiferous tubule lumen appeared, whilst the caput and corpus development coincided temporally with the increase of testicular steroidogenic capacity and tubular fluid secretion. Such findings suggest differential requirements of endocrine and lumicrine stimulation for the normal development of the various anatomical regions of the epididymis.

Keywords: Epididymis; Sexual development; Tropical sheep; Blackbelly lambs

Resumen:

Para caracterizar el desarrollo de los epidídimos, se castraron corderos Blackbelly al nacimiento y cada tres semanas hasta la 21 (n=4 a 6 por grupo). Se registró el peso de los epidídimos y de las tres regiones anatómicas y se tomaron muestras para morfometría. Se calculó el porcentaje de tejido tubular, el diámetro tubular, el grosor y área de la capa muscular, la altura y área del epitelio, y el diámetro y área de la luz tubular. El mayor crecimiento del epidídimo se observó entre las semanas 9 y 18; la cola comenzó a desarrollarse antes que las otras regiones; el peso de ésta fue mayor entre el nacimiento y la semana 12, pero de la semana 15 a la 21 no difirió de la cabeza. En general, el diámetro tubular, el grosor y área de la capa muscular y el diámetro y área de la luz fueron mayores en la cola. La altura del epitelio fue mayor en la cola hasta la semana 9, pero la situación se invirtió a partir de la semana 12. De acuerdo a lo que se conoce de esta raza, la cola comenzó a desarrollarse antes de aparecer la luz de los túbulos seminíferos y del aumento de las concentraciones de testosterona, mientras que el desarrollo de la cabeza y el cuerpo coincidió con el aumento de la capacidad esteroidogénica y la secreción del fluido tubular. Tales hallazgos sugieren diferentes requerimientos de estimulación endocrina y lumicrina para el desarrollo normal de las diferentes regiones del epidídimo.

Palabras clave: Epidídimo; Desarrollo sexual; Ovinos tropicales; Corderos Blackbelly

Introduction

Barbados Blackbelly is a hair breed of sheep (Ovis aries), developed in tropical latitudes and is well adapted to tropical conditions. Ewes are precocious and highly prolific, having a long breeding season1,2. Studies of sexual development and reproductive capacity of Blackbelly males are scarce, albeit the importance of this information for the evaluation, selection and usage of young sires. Testis development is important, as the reproductive capacity and fertility of sires depends primarily on a satisfactory testicular function; however, adequate sperm production must be completed with cell maturation, which is achieved during sperm transit through the epididymis3; any failure during the epididymal development or function might lead to fertility problems, as consequence of maturation disorders, even with adequate sperm production4. Sperm maturation is acquired progressively and simultaneously as the sperm travel through the caput and corpus epididymidis5, whilst the cauda serves primarily as a storage site for functionally mature sperm, since it provides the optimal environment to maintain sperm viability for several days4,5,6.

The functional importance of the anatomical regionalization of the epididymis has been further recognized7, as the several anatomical regions have different patterns of gene and protein expression, in agreement with the different functions relative to sperm maturation and storage. It is expected that the functional differences among the anatomical regions in the adult epididymis are also present in the morphometric characteristics during the development of the epididymal anatomical regions, which could suggest differential requirements and stimulatory mechanisms during their development. Previous information suggests that such differences exist8,9; however, in the first study the only variable studied was the epididymal epithelium, whilst in the last study, the authors used lambs at an age when important developmental changes must have already occurred. A detailed anatomical description would be useful to answer important questions do not solved in the previous studies; therefore, the present is an exploratory study, where quantitative morphometric techniques were used to characterize the development of the several anatomical regions of the epididymides, between birth and 21 wk of age, in Barbados Blackbelly ram lambs.

Material and methods

Animals and experimental design

All the experimental procedures were performed according to the “International Guiding Principles for Biomedical Research Involving Animals” (available at: http://www.cioms.ch/images/stories/CIOMS/IGP2012.pdf). The study was conducted in the state of Queretaro, Mexico (20º 43’ N, 100º 15’ W). Forty-three summerborn (July to September) Barbados Blackbelly ram lambs were used. Lambs were always housed in outdoor pens; before weaning, lambs were creep fed with a diet containing 14 % crude protein (78 % sorghum, 20 % canola meal and 2 % minerals); after weaning at 75 d of age, lambs were offered alfalfa hay and a concentrate as described above, water was always available ad libitum. Lambs were allotted into eight experimental groups, each group were surgically castrated under local anesthesia either, at birth (before 3 d of age), or when they were 3, 6, 9, 12, 15, 18 or 21 wk of age (n= 4 to 6 per group), within each group the difference in age was never greater than 3 d. All castrations were performed during September to December.

Tissue collection and processing

Both epididymides were trimmed off extraneous tissue and weighed separately. The left epididymis was divided in its three anatomical regions, caput, corpus and cauda5. Each region was weighed and the percentage accounted for each region to the whole organ weight was calculated, these percentages were then used to estimate the paired weight of each region. Samples were obtained from the left epididymis, from the zones 2 (caput), 5 (corpus) and 8/9 (cauda)(5), and were fixed and processed for histology10. Three to four sections (5 μm) were made from each sample, mounted onto gelatin-coated glass slides and dried overnight at 37 °C. Sections were stained with hematoxylin-eosin and stored at room temperature until quantitative morphometric analysis was conducted.

Morphometric evaluation of epididymal sections

One or two sections from each epididymal region and ram were randomly chosen and observed under a bright field microscope (Axiostar Plus, Carl Zeiss, Mexico DF); digital images were obtained at 100x or 200x magnifications (depending on the age of the lamb and the variable to be recorded) with a digital camera (Color View II, Soft Imaging System, Lakewood CO) attached to the microscope. Image acquiring and processing were performed using image analysis software (AnalySIS Opti Basic, Soft Imaging System). The percentage of the epididymal parenchyma composed of tubular tissue in each region was determined in images taken at a magnification of 100x. Each section was divided in quadrants, a field from each quadrant was randomly chosen and a square (945.5 x 945.5 μm) was applied; then, all tube sections inside the square were delimited and the software calculated the total tubular area inside the square, which was used to calculate the corresponding percentages. Tubular variables of the epididymal tissue were obtained by tracing outlines of 10 rounded tube sections in every region for each ram lamb, including and not including the muscular layer, also by tracing the tubular lumen. The analysis software calculated several variables, such as tubular area, perimeter and diameter. Such data were used to calculate the tubular diameter, the thickness and area of the muscular layer, the height and area of the epithelium, and the diameter and area of the tubular lumen in every epididymal region in each lamb.

Statistical Analyses

The 10 values for each epididymal region within a lamb were averaged; in this way a single value for a particular epididymal region and lamb was obtained for the statistical analysis. Data were analyzed as a completely randomized design with a factorial arrangement, using the GLM procedure of SAS (SAS Institute Inc., Cary NC, USA). The age of the animals, the anatomical region and the interaction age by region were included in the model; the PDIFF option of SAS was used to compare least square means among age groups and among regions. In order to meet the assumptions of the analysis of variance, percentage data, expressed as proportions (p), were transformed to arc-sine squared root of p; all the other variables were logn transformed. After analysis, data were transformed back to actual values for tables and figures.

Results

Epididymal weight

Differences between ages for paired epididymis weight were always significant (P<0.05), except for 0 vs 3, and 18 vs 21 wk. At birth, the weight of paired epididymides was 0.93 ± 0.07 g (Figure 1), during the first 9 wk increased 5.4 fold (5 ± 0.49 g); the greatest growth rate was observed between 9 and 18 wk (4.7 fold), until reaching 25.6 ± 2.5 g on wk 21. The interaction age x region was significant (P<0.001); paired weight of each epididymal region followed a similar trend, yet with some differences among regions. Corpus epididymidis was always lighter than cauda (P<0.01), and lighter than caput from wk 6 onwards (P<0.01), from 0.14 ± 0.01 g at birth to 4.6 ± 0.31 g at wk 21. At birth, the weight of caput (0.34 ± 0.03 g) and cauda (0.44 ± 0.03 g) were not different to each other, as well as by 3 wk. Between 6 and 12 wk, the cauda weight increased faster and was greater than caput (P<0.01). After wk 12, the caput weight started increasing, in such a way that by 15 to 21 wk no differences were detected between the two regions (caput 10.7 ± 1.03 g; cauda 10.3 ± 0.89 g at wk 21).

Each time point represent the mean ± SE for 4 to 6 rams. *Corpus weight was smaller than caput from 6 wk onwards (P<0.01), and smaller than cauda at every age evaluated (P<0.01). **Cauda weight was larger than caput at 6, 9 and 12 wk of age (P<0.01). The arrow indicates the age when sperm first appeared in the tubular lumen of the three epididymal regions.

Figure 1 Development of paired epididymal weight and paired weight of each anatomical region, from birth to 21 wk of age in Barbados Blackbelly ram lambs. 

The differential development of the epididymal regions was also evident on the percentage that each region accounted to the total organ weight (interaction age x region, P<0.001; Figure 2). The proportion accounted by the caput decreased between birth (36.7 %) and wk 9 (28 %; P<0.001), then increased until wk 15 (P<0.05), with no further changes thereafter until wk 21 (41.7 %). The cauda followed an opposite trend, increasing from birth (47.8 %) to wk 6 (58.5 %; P<0.001), decreasing from wk 9 to 15 (P<0.001), with no further changes thereafter until wk 21 (40.3 %). Cauda was greater than the other regions from birth to wk 12 (P<0.001), and not different from caput at wk 15, 18 and 21; corpus accounted always the smallest percentage (P<0.001).

Each time point represents the mean ± SE for 4 to 6 rams. *Cauda was greater than caput from 0 to 12 wk of age (P<0.001); corpus always accounted for the smaller percentage to the total epididymal weight (P<0.001). The arrow indicates the age when sperm first appeared in the tubular lumen of the three epididymal regions.

Figure 2 Development of the percentage accounted by each epididymal region to the total epididymal weight, from birth to 21 wk of age in Barbados Blackbelly ram lambs. 

Characteristics of the epididymal tissue

Tubular tissue percentage and tubular diameter. The interaction age by region was significant (P<0.05) for the percentage of tubular tissue; this variable had an increasing trend in the three epididymal regions until wk 15 (Table 1); then, it did not change (caput and corpus) or decreased (cauda) by wk 21. Overall, the percentage of tubular tissue was greatest in the cauda and lowest in the caput (P<0.05), except for wk 3, 18 and 21, when no differences among regions were detected; corpus was intermediate, but not always different from the other regions. The increasing rate (percentage of each age, related to wk 21) was different among regions (Figure 3a); by wk 6, corpus and cauda had reached, respectively, 93 and 88 % of the final value, whilst caput had reached only 68 %, such trend was maintained until wk 15. For tubular diameter, the interaction age by region was not significant (P=0.13; Table 1). This variable increased (P<0.05) until wk 15 (caput and corpus) or 12 (cauda), with no changes thereafter. The greatest diameter was always observed in the cauda, and the smallest in the caput (P<005); corpus was not different from caput, except for wk 3 and 6, when all regions were different to each other. Regarding the increasing rate (Figure 3b), by wk 6, caput, corpus and cauda had reached 38, 47 and 55 % of their final values, respectively; similar differences were maintained until wk 12, at that age cauda had reached 92 %, whilst similar percentages (90 %) were not reached in caput and corpus until 18 wk of age.

Table 1 Mean (± SE) of the percentage of tubular tissue and the average tubular diameter in the several epididymal anatomical regions in Barbados Blackbelly ram lambs, from birth to 21 wk of age. 

a-e Means within a column without a common superscript are different (P<0.05).

x,y,z Means within a row and variable without a common superscript are different (P<0.05).

Data are the percentage of the values at each age as compared with the value at 21 wk of age for each variable (panels a, b, d). * For epithelium height (panel c), the percentage value at each age is relative to the maximum value reached in each region (21 wk for caput and corpus, and 9 wk for cauda).

Figure 3 Relative increase of the epididymal tubular tissue percentage (panel a), tubular diameter (panel b), epithelium height (panel c) and epithelium area (panel d) in Barbados Blackbelly ram lambs. 

Epididymal muscular layer. The interaction age by region was significant (P<0.01) for both variables of the muscular layer. The thickness of the muscular layer in caput did not change between birth and wk 6 (Table 2), increased 35 % by wk 9 (P<0.05) and then, did not change or had a descendent trend until wk 21. In the cauda, the muscular thickness did not change between birth and wk 6, increased 119 % by wk 9 (P<0.05), with no change by wk 15 and a descendent trend thereafter (P<0.05). In the corpus epididymidis there were no changes between 3 and 21 wk. When comparing the muscular layer thickness in wk 0 vs wk 21, no differences were observed in the caput and corpus, but in the cauda, it was 48 % greater on wk 21 (P<0.05). The muscular layer area (Table 2) increased until wk 12 (caput and corpus) and 9 (cauda), with no significant changes thereafter. The maximum area observed in each region, as compared to value at birth, was 3.8-, 3.8-, and 5.5-fold, for caput (wk 18), corpus (wk 18) and cauda (wk 15), respectively. Comparisons among regions were similar for both variables, the greatest values were observed in the cauda (P<0.05), followed by the corpus and caput; however, differences between the last two were significant (P<0.05) only at 3 and 6 wk.

Table 2 Mean (± SE) of the thickness and area of the tubular muscular layer in the several epididymal anatomical regions in Barbados Blackbelly ram lambs, from birth to 21 wk of age. 

a-e Means within a column without a common superscript are different (P<0.05).

x,y,z Means within a row and variable without a common superscript are different (P<0.05).

Epididymal epithelium. The interaction age by region was significant (P<0.001) for both variables of the epithelial layer. In the caput and corpus, the epithelium height did not change between birth and wk 6, then increased until wk 12 (caput) or 15 (corpus), with no further changes (Table 3); in the cauda, an increasing trend was observed from birth to wk 9, then, decreased on wk 12, with no more changes until wk 21. Comparison between regions had two different phases, from birth to wk 9, the epithelium was highest in the cauda and lowest in the caput (P<0.05), but from 12 to 21 wk the situation reversed, as the lowest values were observed in the cauda (P<0.05) and the greatest in the caput and corpus with no differences between the last two. Regarding the increasing rate (Figure 3c), at birth, cauda had over 45 % of their maximum value, which was reached at wk 9; caput and corpus, at birth had reached, respectively, 20 and 25 % of the value at wk 21, and did not reach over 90 % until wk 15. The epithelial area (Table 3) did not change between birth and wk 6 (caput and corpus) or 3 (cauda), then, it increased until wk 15 in the three regions (P<0.05), with no further changes (Table 3). Between birth and wk 12, the greatest values were observed in the cauda, with the smallest values in the caput (P<0.05); from wk 15 onwards no differences among regions were detected. The increasing rate was always greater for cauda (Figure 3d), by wk 6 it had reached 31 %, as compared with 5 and 8 % for caput and corpus, respectively; such differences were maintained until wk 18.

Table 3 Mean (± SE) of the tubular epithelium height and area in the several epididymal anatomical regions in Barbados Blackbelly ram lambs, from birth to 21 wk of age. 

a-d Means within a column without a common superscript are different (P<0.05).

x,y,z Means within a row and variable without a common superscript are different (P<0.05).

Epididymal tubular lumen. The interaction age by region was not significant (P≥0.25) for both variables of the tubular lumen, but the effect of region was (P<0.001). The lumen diameter and area did not increase or increased very little in all three regions until wk 6; then, increased steadily until wk 15 (caput and corpus) or 12 (cauda), with no further changes thereafter (Table 4). The greatest relative augment was observed between 9 and 12 wk (0.5- to 1.2-fold in the lumen diameter, and 1.3- to 5.2-fold in the lumen area), with the greatest increase in the cauda; both variables were greatest in the cauda at all ages (P<0.05), with no differences between caput and corpus. The maximum lumen diameter observed in each region (caput, corpus and cauda, respectively) corresponded to 3.7-, 3.5- and 5.2-fold increase, as compared to wk 0. Similarly, the increase in the lumen area represented 21.8-, 21.2- and 24.9-fold, as compared to wk 0, for caput, corpus and cauda, respectively. Sperm first appeared in the tubular lumen of the three epididymal regions by wk 18 (arrows in Figures 1 and 2), which indicate that by that age the lambs had already reached or were very close to reach puberty.

Table 4 Mean (± SE) of the tubular lumen diameter and area in the several epididymal anatomical regions in Barbados Blackbelly ram lambs, from birth to 21 wk of age. 

a-d Means within a column without a common superscript are different (P<0.05).

y,z Means within a row and variable without a common superscript are different (P<0.05).

Discussion

Epididymal growth followed a parallel trend to testis development, as reported previously for Blackbelly ram lambs10; the greatest relative epididymal growth was observed between 9 and 18 wk, which agrees temporally with the greatest rate of testicular growth in this breed10,11. During that stage of development, the absolute increase of the interstitial tissue in the testis is associated with increased number of Leydig cells and with the development of their steroidogenic capacity12. This, in turn, leads to increased plasma concentrations of testosterone10,13 and, therefore, to greater stimulation to the epididymides, as the development and function of these organs depend on adequate androgen contribution14,15.

The functional component of the epididymis is the tubular tissue, as all the changes related to sperm maturation and storage during their transit through the epididymis take place in the luminal compartment, under a highly specialized microenvironment consequence of the epithelial activity4,5. To accomplish this task, the epithelium must be structured in a way such that prevent and regulate the entry of substances into the lumen, it has the ability of synthesize, secrete and absorb components, and it is arranged so that the sperm come into contact with the appropriate environment at the appropriate time16. It is, therefore, reasonable to consider the variables related to tubular tissue and epithelial layer as the most appropriate to evaluate the epididymal development at the microscopic level; such variables have been used to evaluate epididymal function in several experimental models15,17,18.

At the macroscopic level (weight and relative contribution to the whole organ weight), the development of the several anatomical regions of the epididymides followed a different trend to each other; the cauda epididymidis began to develop at a very early age (wk 6), whereas the greatest development of the caput and corpus started by wk 12. The findings in the present study, at both, the macroscopic and microscopic levels, suggest that the postnatal development of the epididymides goes from the cauda towards the caput, which agrees with data reported for other species, such as cattle19, goats17 and rats16. In sheep there is some discrepancy in this matter; whereas some authors reported a trend similar to that observed in the present study8, others9 found a maturation process advancing from caput to cauda. It is highly probable that the age of the experimental animals used in the different studies in lambs had accounted for the variation of the results observed among studies. In the study of Bielli9, ram lambs were older (90 to 180 d-old, that is, 12.9 to 25.7 wk), as compared with lambs in the study of Nilnophakoon8 (1 to 18 wk) and ours (birth to 21 wk). This fact determines important differences in the stage of physiological maturity of the lambs at the beginning of those studies, as important anatomical and physiological changes occur in the testes and epididymides before 12 wk of age10,13.

Epididymal function does not depend only on the endocrine stimulation received from testosterone in blood; even more important might be the lumicrine system7,15, given by testosterone and other factors15,16. Testosterone, bound to the androgen binding protein (ABP), reaches the epididymides via the efferent ducts, where it is converted into dihydrotestosterone20. In addition, several growth factors contained in the tubular fluid have important effects on epididymal function15,16,21; these factors are produced by the Sertoli cells in the seminiferous tubules22, and carried towards the epididymides via the excurrent duct system. Then, fluid composition undergoes modifications as travels through the epididymal duct5,16. Such lumicrine regulation is feasible only after the seminiferous tubule lumen appears, as result of increased fluid secretion by Sertoli cells, when they initiate the maturation process to acquire their functional capacity as adult cells22. In Blackbelly ram lambs the lumen of the seminiferous tubules appears after 9 wk of age, and by wk 12 lumen is present in 80 % of the tubules10. This finding also coincides temporarily with the greatest increase in epididymal weight, and with the greatest increase of the epithelium height in the caput and corpus epididymidis observed in the present study, which is in agreement with previous reports in sheep8 and goats23.

Cauda epididymidis began to develop before the accelerated growth of the testes10. At that time, there is still no contribution of tubular fluid via the testicular excurrent duct system, because the lumen of the seminiferous tubules has not formed yet10. Such findings suggest that the initial development of the cauda epididymidis could not depend on the presence of testosterone or other luminal factors coming from the testicular tubular system. Additional evidences supporting this possibility have been presented in studies with mature goats, whose efferent ducts had been ligated23; in these goats, it was evident the lack of morphologic and functional dependence of the cauda epididymidis towards the secretions coming from the testis, via the extra testicular excurrent duct system23. When cauda epididymidis began to develop, plasma concentration of testosterone must have been still very small10,13; therefore, initial caudal development might not depend on high testosterone concentrations, or depend on other predominant steroids different from testosterone, such as androstenedione, whose circulating concentrations are larger at that age24,25,26. Another possibility is that the threshold of the caudal response to testosterone and other circulating androgens might be lower at that age.

Conclusions and implications

In conclusion, data of the present study indicate that the pattern of development of the epididymis in sheep is regionalized, going from cauda to caput, that is, the cauda started developing earlier than the other anatomical regions. The development of cauda epididymidis should have started before the increase of testosterone concentration in blood plasma, and before the seminiferous tubule lumen appeared; in contrast, the caput and corpus development should have coincided temporally with the increase of the testicular steroidogenic capacity and tubular fluid secretion. Such findings suggest that the various anatomical regions of the epididymis have differential requirements of endocrine and lumicrine stimulation for their normal development.

Acknowledgements

To the “Consejo Nacional de Ciencia y Tecnología”, México, for financing the project (39290-B); Víctor Robledo and Adolfo Paulín, from the “Universidad Autónoma de Querétaro” (UAQ), for providing with, and caring for the lambs; Jesús Herrera for helping in tissue collection; Miguel Silva and Mary Guerrero (UAQ) for tissue processing. AD Vargas-Velázquez is a former student, under the supervision of the last author (HJS).

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Received: March 19, 2015; Accepted: April 23, 2015

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