Immediate and late effects of long-term testicular heat stress on the number of seminiferous tubules and cellular content in Santa Inês rams

Luana Vanessa Ribeiro; Bárbara Rost Dalchiavon; Mayra Elena Ortiz D´Ávila Assumpção; Thais Rose dos Santos Hamilton

doi:10.1590/1984-3143-AR2024-0134

SHORT COMMUNICATION

Immediate and late effects of long-term testicular heat stress on the number of seminiferous tubules and cellular content in Santa Inês rams

Luana Vanessa Ribeiro; Bárbara Rost Dalchiavon; Mayra Elena Ortiz D´Ávila Assumpção; Thais Rose dos Santos Hamilton

http://dx.doi.org/10.1590/1984-3143-AR2024-0134 Anim Reprod, vol.22, n4, e20240134, 2025

PDF

Downloads: 2

Abstract

Efficient spermatogenesis in mammals occurs when testicular temperature is approximately 2 to 8 °C below body temperature. Elevated testicular temperature can trigger oxidative stress and compromise sperm integrity during spermatogenesis, potentially resulting in damaged spermatozoa and male infertility. This study aimed to evaluate how heat stress affects the quantity of seminiferous tubules, and the abundance of germ cells within the seminiferous tubules. To this end, six Santa Inês rams were subjected to testicular insulation for 12 consecutive days, followed by two hemi-orchiectomies, the first 24 hours after insulation period to evaluate the immediate effect, and the second 30 days after the first hemi-orchiectomy to evaluate the late effect. Six Santa Inês rams composed the control group. Histological analyses were conducted to quantify the number of seminiferous tubules and the types of cells within them (spermatogonia, spermatocytes, and spermatids) in testicular fragments. Despite an increase in testicular temperature, no significant differences were observed in the number of seminiferous tubules. These findings probably reflect the resistance of Santa Ines rams to high environment temperatures. Regarding the abundance of cells, a decrease in spermatogonia (0.27% ± 0.06; 0.05% ± 0.03, p = 0.005) and an increase in spermatocytes (35.90% ± 1.58; 46.77% ± 4.33, p = 0.028) were observed immediately after the insulation period compared to 30 days after, the late effect. This result suggests an effect of the first hemi-orchiectomy on the remaining testicle, probably an attempt to maintain sperm production.

Keywords

spermatogenesis, testicular insulation, spermatogonia, spermatocyte, orchiectomy

References

Ahn JS, Kwon EG, Lee HJ, Lee EM, Hwang SM, Cho SR, Kim KW, Kim UH, Won J, Jin S, Kang SS, Park BK, Jang GS, Jang SS. Effect of hemi-castration on the productivity, histological characteristics, and economic efficacy of Korean Beef Catle. Animals (Basel). 2021;11(9):2490-501. http://doi.org/10.3390/ani11092490. PMid:34573457.

Almeida MM, Carvalho MAM, Machado AAN Jr, Righi DA, Xavier FG, Conde Júnior AM, Bombonato PP. Effect of the scrotal division degrees on the arterial supply distribution of native goats from the Piaui State. Braz J Vet Res Anim Sci. 2008;45(3):167-75. http://doi.org/10.11606/issn.1678-4456.bjvras.2008.26693.

Asadi N, Bahmani M, Kheradmand A, Rafieian-Kopaei M. The impact of oxidative stress on testicular function and the role of antioxidants in improving it: a review. J Clin Diagn Res. 2017;11(5):IE01-05. http://doi.org/10.7860/JCDR/2017/23927.9886. PMid:28658802.

Correa MPC, Dallago BSL, Paiva SR, Canozzi MEA, Louvandini H, Barcellos JJ, McManus C. Multivariate analysis of heat tolerance characteristics in Santa Inês and crossbred lambs in the Federal District of Brazil. Trop Anim Health Prod. 2013;45(6):1407-14. http://doi.org/10.1007/s11250-013-0378-3. PMid:23456786.

Dutta S, Sengupta P, Siama P, Roychoudhury S. Oxidative stress, testicular inflammatory pathways, and male reproduction. Int J Mol Sci. 2021;22(18):10043. http://doi.org/10.3390/ijms221810043. PMid:34576205.

Fleming JS, Yu F, McDonald RM, Meyers SA, Montgomery GW, Smith JF, Nicholson HD. Effects of scrotal heating on sperm surface protein PH-20 expression in sheep. Mol Reprod Dev. 2004;68(1):103-14. http://doi.org/10.1002/mrd.20049. PMid:15039954.

Gonen N, Quinn A, O’Neill H, Koopman P, Lovell-Badge R. Normal levels of SOX9 expression in the developing mouse testis depend on the TES/TESCO enhancer, but this does not act alone. PLoS Genet. 2017;13(1):e1006520. http://doi.org/10.1371/journal.pgen.1006520. PMid:28045957.

Hamilton TRS, Assumpção MEOD. Sperm DNA fragmentation: causes and identification. Zygote. 2020;28(1):1-8. http://doi.org/10.1017/S0967199419000595. PMid:31603068.

Hamilton TRS, Mendes CM, Castro LS, Assis PM, Siqueira AFP, Delgado JC, Goissis MD, Muiño-Blanco T, Cebrián-Pérez JA, Nichi M, Visintin JA, Assumpção MEOD. Evaluation of lasting effects of heat stress on sperm profile and oxidative status of ram semen and epididymal sperm. Oxid Med Cell Longev. 2016;2016:1687657. http://doi.org/10.1155/2016/1687657. PMid:26881013.

Hamilton TRS, Siqueira AP, Castro LS, Mendes CM, Delgado JC, Assis PM, Mesquita LP, Maiorka PC, Nichi M, Goissis MD, Visintin JA, Assumpção MEOD. Effect of heat stress on sperm DNA: protamine assessment in ram spermatozoa and testicle. Oxid Med Cell Longev. 2018;2018:5413056. http://doi.org/10.1155/2018/5413056. PMid:29765499.

McMillan DB, Harris RJ. An atlas of comparative vertebrate histology. Kidlington, United Kingdom: Elsevier; 2018.

Ming Z, Vining B, Bagheri-Fam S, Harley V. SOX9 in organogenesis: shared and unique transcriptional functions. Cell Mol Life Sci. 2022;79(10):522. http://doi.org/10.1007/s00018-022-04543-4.

Moore KL, Persaud TVN, Torchia MG. Before we are born essentials of Embriology and Birth Defects. 7th ed. Philadelphia: Saunders Elsevier; 2013.

Nichi M, Bols PEJ, Zuge RM, Barnabe VH, Goovaerts IGF, Barnabe RC, Cortada CNM. Seasonal variation in semen quality in Bos indicus and Bos taurus bulls raised under tropical conditions. Theriogenology. 2006;66(4):822-8. http://doi.org/10.1016/j.theriogenology.2006.01.056. PMid:16529802.

Paul C, Teng S, Saunders PTK. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod. 2009;80(5):913-9. http://doi.org/10.1095/biolreprod.108.071779. PMid:19144962.

Reviello JS. Embriologia veterinária. Rio de Janeiro: Freitas Bastos; 2024.

Rizzoto G, Hall C, Tyberg JV, Thundathil JC, Caulkett NA, Kastelic JP. Increased testicular blood flow maintains oxygen delivery and avoids testicular hypoxia in response to reduced oxygen contente in inspired air. Sci Rep. 2018;8(1):10905. http://doi.org/10.1038/s41598-018-29248-2. PMid:30026599.

Robinson BR, Netherton JK, Ogle RA, Baker MQ. Testicular heat stress, a historical perspective and two postulates for why male germ cells are heat sensitive. Biol Rev Camb Philos Soc. 2023;98(2):603-22. http://doi.org/10.1111/brv.12921. PMid:36412227.

Saleh RA, Agarwal A. Oxidative stress and male infertility: from research bench to clinical practice. J Androl. 2002;23(6):737-52. http://doi.org/10.1002/j.1939-4640.2002.tb02324.x. PMid:12399514.

Senger PL. Pathways to pregnancy and parturition. 3rd ed. Washington: Current Conceptions; 2005.

Tsakmakidis IA. Ram semen evaluation: development and efficiency of modern techniques. Small Rumin Res. 2010;92(1-3):126-30. http://doi.org/10.1016/j.smallrumres.2010.04.017.

Valencise L, Ferreira ASBS, Mazzoni TS, Kempinas WG. Embriologia animal: referência e atlas. Botucatu: Unesp/IBB; 2021.

Van Camp SD. Common causes of infertility in the bull. Vet Clin North Am Food Anim Pract. 1997;13(2):203-32. http://doi.org/10.1016/S0749-0720(15)30336-4.

Walczak-Jedrzejowska R, Wolski JK, Slowikowska-Hilczer J. The role of oxidative stress and antioxidants in male fertility. Cent European J Urol. 2013;66(1):60-7. http://doi.org/10.5173/ceju.2013.01.art19.

Zhang J, Ricketts SW, Tanner SJ. Antisperm antibodies in the semen of a stallion following testicular trauma. Equine Vet J. 1990;22:138-41. http://doi.org/10.1111/j.2042-3306.1990.tb04228.x.

Zhang M, Liu Q, Meng H, Duan H, Liu X, Wu J, Gao F, Wang S, Tan R, Yuan J. Ischemia-reperfusion injury: molecular mechanisms and therapeutic targets. Signal Transduct Target Ther. 2024;9(1):12. http://doi.org/10.1038/s41392-024-02041-6. PMid:38185705.

Submitted date:
12/03/2024

Accepted date:
07/11/2025

Immediate and late effects of long-term testicular heat stress on the number of seminiferous tubules and cellular content in Santa Inês rams

Luana Vanessa Ribeiro; Bárbara Rost Dalchiavon; Mayra Elena Ortiz D´Ávila Assumpção; Thais Rose dos Santos Hamilton

Abstract

Keywords

References

Links

Share

Anim Reprod