a,b = average values, followed by different small letters on the same line, differ between each other by Tukey’s test (P < 0.05), A,B = average values of the same parameter, followed by capital letters in the same column, differ between each other by Tukey’s test (P < 0.05). LT = left testicle, RT = right testicle. *Average of the left and right testicles.

Figure 1. Ultrasound images of the testicular parenchyma and mediastinum of Texel rams. Square area = 1600 mm2.

Table 2. Correlations between the average intensity of pixels in the area of 1600 mm2 and quality parameters of the ejaculate of Texel rams.

MOT = straight-line progressive spermatic motility; VIG = spermatozoon vigor; MDEF = % of major defects; MINDEF = % of minor defects; TDEF = % of total defects; SD = standard deviation; NS = no significant correlation.

Table 3. Number of Texel rams with fibrotic lesions in the testis.

Table 4. Correlations of the fibrosis score of the right testicle, age, testicular consistency and physical and morphological parameters of the ejaculate.

FSRT = fibrosis score of the right testicle; CONS = consistency; TURB = turbulence; MOT = spermatic motility; VIG = spermatic vigor; MDEF = major defects; MINDEF = minor defects; TDEF = total defects. **Correlation is significant at a level of 0.01. *Correlation is significant at a level of 0.05. NS = no significant correlation.

The number of animals with fibrotic lesions in the testis is presented in Table 3. Among the animals that had fibrosis in both testicles, 81% had scores of 1/1, 13% scores of 1/2, and 6% scores of 2/1, for the left/right testicles, respectively.

No correlations were found between the fibrosis score and the physical and morphological parameters of the semen (Table 4 and Table 5).

A total of 85% (75/88) of the animals were classified as being able to reproduction, while 15% (13/88) were deemed unable to reproduction. The results of the testicular echotexture of the left and right testicles, and the average of the two testicles, according to these two subgroups, are summarized in Table 6. There was no difference in the IP of the studied testicular images (P > 0.05) between able and unable animals.

As expected, the evaluated parameters were considered the most optimal in animals classified as able to reproduce, showing a difference only in motility and spermatic vigor between the two classes (P < 0.05).

4. Discussion

In the scientific literature, apart from the present study, there is no previous report regarding testicular echotexture of rams of the Texel breed, with research on hair sheep, particularly the Santa Inês breed, being the most widespread. Jucá et al. [9] characterized the echotexture of the testicles of young ovines in the phase of testicular maturation by assessing Santa Inês rams at weaning. They found no differences in echogenicity in the evaluations of the parenchyma and calcifications between the right and left testicles, classifying 90.24% of the images as hypoechoic with low-intensity (IP 111) and 9.76% as hypoechoic with high intensity (IP 12), and correlating these findings with the ages of the animals. Andrade et al. [10] demonstrated homogeneous testicular parenchyma, with the

Table 5. Correlations of the fibrosis score of the left testicle, age, and physical and morphological parameters of the ejaculate.

FSLT = fibrosis score of the left testicle; CONS = consistency; TURB = turbulence; MOT = straight-line progressive spermatic motility; VIG = spermatic vigor; MDEF = major defects; MINDEF = minor defects; TDEF = total defects. **Correlation is significant at a level of 0.01. *Correlation is significant at a level of 0.05. NS = no significant correlation.

Table 6. Intensity of pixels of the testicles of Texel rams, classified as able and unable to reproduction.

a,b = average values, followed by different small letters on the same line, differ between each other by Tukey’s test (P < 0.05). A,B = average values of the same parameter, followed by capital letters in the same column, differ between each other by Tukey’s test (P < 0.05).

echogenicity ranging from low to moderate, regardless of the testicle (right or left) and the scanning plane used. Instead, they found that the echogenicity increased in direct proportion to the age of the animals, corroborating the results of Cartee et al. [11] , and Moura et al. [12] .

A similar result was observed in the present study, in which the average intensities of the pixels according to the representative area of the predetermined testicular regions on the ultrasound images, were found to be moderately echogenic relative to the gray scale used (0 - 255). This result may be related to the stage of sexual maturity of the rams studied (end of puberty and beginning of sexual maturity), and the anatomical changes of the seminiferous tubules, which, according to Aravindakshan et al. [13] , and Hamm and Fobbe [14] , become longer and twisted, increasing in diameter, and forming the lumen [14] , as a result of the increased thickness of the basement membrane during this period. This suggests the possibility of using ultrasonography to monitor the progressive changes that occur in the testicles [7] , as well as the homogeneity of the lot.

Based on this knowledge and the fact that no correlation was found between the seminal characteristics and the IP values of the studied images, Arteaga et al. [15] stated that testicular ultrasonography is better associated with future seminal patterns than with the characteristics of the semen at the time of ultrasound evaluation. However, this finding is likely due to the lack of correlation found by these authors between testicular echotexture and seminal characteristics, since they only observed the IP correlation with seminal characteristics from two to four weeks after the ultrasound examination, and not with the seminal characteristics at the time of ultrasound evaluation.

Regarding the identification of testicular alterations, there was no correlation between the degree of testicular impairment and the observed fibrosis score with the seminal characteristics (P > 0.05) of the rams in the present study. However, significant correlations were observed between the fibrosis score and age (P < 0.01).

Barth et al. [16] observed no difference in the fibrosis score between the left and right testicles. These same authors, when evaluating 175 bulls (Bos taurus taurus), aged between 10 and 12 months old, observed that 70% presented some testicular fibrosis impairment; of these, 15.4% had moderate to severe fibrosis, with compromised the spermatic quality. Conversely, when evaluating bulls of 18 - 20 months of age (n = 105), the authors observed no association between the severity of fibrotic lesions and seminal characteristics.

Chapwanya et al. [17] and Gnemmi and Lefebvre [18] also identified palpable and non-palpable lesions, indicating that testicular ultrasound is a more sensitive and reliable mode of diagnosis than palpation alone, whereas Chapwanya et al. [17] , studying 32 bulls with an average age of 5.6 years, identified seven bulls with testicular lesions detected by ultrasonography, with two of them having levels of testicular fibrosis that could compromise seminal quality.

The degree of severity of fibrotic lesions measured in the testicles of the animals evaluated in this present study was not associated with low quality semen. Likewise, Barth et al. [16] noted that even bulls with very severe degrees of fibrosis produced semen with up to 94% morphologically normal spermatozoa. These results indicate that the presence of relatively large amounts of scar tissue within the testicular parenchyma does not necessarily prevent the production of normal spermatozoa by other areas of the testicular parenchyma. According to the authors, large amounts of scar tissue would be needed to reduce spermatic production.

The present study showed that 85% of animals were able to reproduction, while 15% were unable to reproduction. However, no difference was found in the IP between the testicles, or between the classes of rams able and unable to reproduction (P > 0.05), corroborating the results of the studies by Aravindakshan et al. [12] and Cardilli et al. [19] , which found no differences in the IP for the left and right testicles of bovines.

The observed differences (P < 0.05) in physical semen parameters (motility and vigor) between the classes were expected, since the spermatic morphology was the main criterion used for and urological classification, and since the rams were classified as unable only by spermiogram and not by any other reproductive clinical findings.

Further, in the present study, the SC and BCS did not present significant differences (P > 0.05) between able and unable classes, with average values of 28.6 cm and 3.51 for animals able to reproducing, and 27.7 cm and 3.34 for animals unable to reproduction, respectively. Although a difference in SC in relation to the and urological classes studied was not observed (P > 0.05), according to Guimarães et al. [20] , breeding animals with elevated SC are more likely to present satisfactory BSE in relation to those with lower SC. However, this fact has low correlation in adult animals, being high only in growing animals.

The existence of a correlation between SC and reproductive characteristics in ovines, confirmed by Land [21] , and later by Notter et al. [22] , may be considered when choosing the breeding animal. This assertion corroborates the findings of Moraes et al. [23] , when evaluating the fertility of ovines of the Corriedale breed, aged from 12 to 24 months, and using a SC greater than 29 cm as the reference. The authors concluded that there exists a margin of security of 90% in choosing rams based on this characteristic.

According to Cardoso and Queiroz [24] , SC also provides a substantial amount of information on the reproductive capacity of ovines, emphasizing its importance within the testicular morphometry and its usefulness as a component in the selection of rams.

Freitas et al. [25] evaluated hair ovines of Santa Inês, Somali, and Morada Nova breeds, from 6 to 36 months of age, with the SC ranging from 24 to 33 cm, and concluded that this parameter is related to the weight and age of the animals, and that those that do not present the expected SC for their reproductive age should be discarded. Furthermore, Souza and Costa [26] noted in hair ovines of mixed breed, with an average SC of 24.4 cm, a high correlation between this parameter and body weight, concluding that the choice of the ram can be made based on one of these parameters.

Moreover, in studies with ovines of the Hampshire Down breed and their crosses, Mies Filho et al. [27] observed that all the pure-bred lambs presented spermatozoa at six months of age, always being heavier and with an SC of about 26.0 cm, which did not occur with the mixed breeds, although spermatozoa were found in such animals with a scrotal circumference of at least 27.0 cm; spermatogenesis really established itself when the animals presented a scrotal circumference of 28.0 cm.

5. Conclusion

In conclusion, the smallest representative area to evaluate the echo texture of the testicular parenchyma of ovines was found to be 1600 mm2, and there were no correlations between the intensity of pixels of the testicular parenchyma and fibrosis score with the physical and morphological characteristics of the ejaculate of the rams.

Conflict of Interests

The authors declare that have no conflict of interests.

Cite this paper
Urt, M. , Bakarji, E. , Faria, F. , Santos, E. and Costa, D. (2018) Lack of Relationship between Testicular Echotexture and Seminal Characteristics in Adult Texel Rams. Agricultural Sciences, 9, 936-946. doi: 10.4236/as.2018.98065.
References
[1]   King, A.M. (2006) Development, Advances and Applications of Diagnostic Ultrasound in Animals. The Veterinary Journal, 171, 408-420.
https://doi.org/10.1016/j.tvjl.2004.10.014

[2]   Ginther, O.J. (1986) Ultrasonic Imaging and Reproductive Events in the Mare. 3rd Edition, University of Wisconsin, Madison.

[3]   Singh, J., Pierson, R.A. and Adams, G.P. (1998) Ultrasound Image Attributes of Bovine Ovarian Follicles and Endocrine and Functional Correlates. Journal of Reproduction and Fertility, 12, 19-29.
http://www.reproduction-online.org/content/112/1/19.long
https://doi.org/10.1530/jrf.0.1120019


[4]   Pierson, R.A. and Adams, G.P. (1995) Computer-Assisted Image Analysis, Diagnostic Ultrasonography and Ovulation Induction: Strange Bedfellows. Theriogenology, 43, 105-112.
https://doi.org/10.1016/0093-691X(94)00014-L

[5]   Singh, J., Adams, G.P. and Pierson, R.A. (2003) Promise of New Imaging Technologies for Assessing Ovarian Function. Animal Reproduction Science, 78, 371-399.
https://doi.org/10.1016/S0378-4320(03)00100-3

[6]   Jefferies, W.M. (1961) Occult Hypothyroidism and Metabolic Insufficiency. Journal of Chronic Diseases, 4, 582-592.
https://doi.org/10.1016/0021-9681(61)90022-4

[7]   Pinho, R.O., Costa, D.S., Siqueira, J.B., Martins, L.F., Miranda Neto, T., Pereira, J.V.T.N., Guimarães, S.E.F. and Guimarães, J.D. (2013) Testicular Fibrotic Lesions and Semen Quality in Adult Montana Tropical Compound bulls. Revista Brasileira de Medicina Veterinaria, 35, 105-110.
http://rbmv.org/index.php/BJVM/article/view/602/466

[8]   CBRA—Colégio Brasileiro de Reprodução Animal (2013) Manual for Breeding Soundness Examination. 3rd Edition, Belo Horizonte.

[9]   Jucá, A.F., Pinto, L.F.B., Moita, A.K.F., Oliveira, R.J.F., Melo Filho, G.M., Santos, L.B., Fiuza, M.S. and Azevedo, H.C. (2011) Testicular Ecotexture by Ultrasonography in Santa Inês Rams. Proceedings of XXI Congresso Brasileiro de Zootecnia, Maceió, 23-27 May 2011, 1-3.

[10]   Andrade, A.K.G., Soares, A.T., Cartaxo, F.Q., Peña-Alfaro, C.E. and Guerra, M.M.P. (2012) Ultrasonographic Findings in the Testis and Epididymis of Clinically Healthy Young Hair Sheep. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 64, 371-379.
https://doi.org/10.1590/S0102-09352012000200017

[11]   Cartee, R.E., Rumph, P.F., Abuzaid, S. and Carson, R. (1990) Ultrasonographic Examination and Measurement of Ram Testicles. Theriogenology, 33, 867-875.
https://doi.org/10.1016/0093-691X(90)90822-B

[12]   Moura, J.C.A., Jucá, A.F., Gusmão, A.L., Bittencourt, T., Pinho, T.G. and Barbosa, C.M.P. (2008) Testicular Ecotexture of the Santa Inês Rams. A Hora Veterinária, 27, 9-22.

[13]   Aravindakshan, J.P., Honaramooz, A., Bartlewski, P.M., Beard, A.P., Pierson, R.A. and Rawlings, N.C. (2000) Pattern of Gonadotropin Secretion and Ultrasonographic Evaluation of Developmental Changes in the Testis of Early and Late Maturing Bull Calves. Theriogenology, 54, 339-354.
https://doi.org/10.1016/S0093-691X(00)00353-8

[14]   Hamm, B. and Fobbe, F. (1995) Maturation of the Testis: Ultrasound Evaluation. Ultrasound in Medicine and Biology, 21, 143-147.
https://doi.org/10.1016/S0301-5629(94)00088-3

[15]   Arteaga, A.A., Barth, A.D. and Brito, L.F. (2005) Relationship between Semen Quality and Pixel-Intensity of Testicular Ultrasonograms after Scrotal Insulation in Beef Bulls. Theriogenology, 64, 408-415.
https://doi.org/10.1016/j.theriogenology.2004.12.008

[16]   Barth, A.D., Alisio, L., Avilés, M., Arteaga, A.A., Campbell, J.R. and Hendrick, S.H. (2008) Fibrotic Lesions in the Testis of Bulls and Relationship to Semen Quality. Animal Reproduction Science, 106, 274-288.
https://doi.org/10.1016/j.anireprosci.2007.05.002

[17]   Chapwanya, A., Callanan, J., Larkin, H., Keenan, L. and Vaughan, L. (2008) Breeding Soundness Evaluation of Bulls by Semen Analysis, Testicular Fine Needle Aspiration Cytology and Trans-Scrotal Ultrasonography. Irish Veterinary Journal, 61, 315-318.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3113862/pdf/
2046-0481-61-5-315.pdf


[18]   Gnemmi, G. and Lefebvre, R.C. (2009) Ultrasound Imaging of the Bull Reproductive Tract: An Important Field of Expertise for Veterinarians. Veterinary Clinics of North America: Food Animal Practice, 25, 767-779.
https://doi.org/10.1016/j.cvfa.2009.07.006

[19]   Cardilli, D.J., Toniollo, G.H., Pastore, A.A., Canola, C.J. and Mercadante, M.E.Z. (2009) Ultrasonographic Changes of the Testicular Parenchyma Pattern in Young Nelore Bulls. Acta Scientiae Veterinariae, 37, 367-370.
http://www.ufrgs.br/actavet/37-4/Art%20858.pdf

[20]   Guimarães, J.D., Vasconcelos, C.O., Guimarães, S.E.F., Costa, E.P. and Miranda Neto, T. (2003) Testicular Biometry in Nellore Bulls, from 20 to 22 Months of Age. Revista Brasileirade Reprodução Animal, 27, 173-174.

[21]   Land, R.B. (1973) The Expression of Female Sex-Limited Characters in the Male. Nature, 241, 208-209.
https://www.nature.com/articles/241208a0

[22]   Notter, D.R., Lucas, J.R. and McClaugherty, F.S. (1981) Accuracy of Estimation of Testis Weight from in Situ Testis Measures in Ram Lambs. Theriogenology, 15, 227-234.
https://doi.org/10.1016/S0093-691X(81)80011-8

[23]   Moraes, J.C.F., Silva, J.F. and Ferreira, J.M.M. (1985) Seasonal Variation of the Scrotal Perimeter in Corriedale Lambs. Proceedings of VI Simpósio Nacional de Reprodução Animal, Belo Horizonte, 15-19 July 985, 423-424.

[24]   Cardoso, F.M. and Queiroz, G.F. (1988) Duration of the Cycle of the Seminiferous Epithelium and Daily Sperm Production of Brazilian Hairy Rams. Animal Reproduction Science, 17, 77-84.
https://doi.org/10.1016/0378-4320(88)90047-4

[25]   Freitas, V.J.F., Lima, F.R.G. and Paiva, H.M. (1991) Testicular Biometry of Goats and Sheep Raised in the State of Ceará. Revista Ciencia Animal, 1, 51-63.

[26]   Souza, I.A.T. and Costa, F.A.L. (1992) Semen Characteristics and Correlation with Other Reproductive Parameters in Rams. Proceedings of V Simpósio em Ciências Agrárias, Teresina, 2-5 July 1992, 80-86.

[27]   Mies Filho, A., Jobim, M.I.M., Oberst, E.R. and Wald, V.B. (1993) Seasonal Variation of Sperm Production and Scrotal Perimeter of Hampshire down Rams. A Hora Veterinária, 13, 53-57.

 
 
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