Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Testicular hyperthermia increases blood flow that maintains aerobic metabolism in rams

G. Rizzoto https://orcid.org/0000-0002-9423-9658 A , C. Hall B , J. V. Tyberg B , J. C. Thundathil A , N. A. Caulkett C and J. P. Kastelic A D
+ Author Affiliations
- Author Affiliations

A Department of Production Animal Health, Faculty of Veterinary Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, AB T2N 4N1, Canada.

B Departments of Cardiac Sciences and Physiology and Pharmacology, Libin Cardiovascular Institute of Alberta, University of Calgary, 3330 Hospital Drive NW, Calgary, AB T2N 4N1, Canada.

C Department of Veterinary Clinical and Diagnostic Sciences, Faculty of Veterinary Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, AB T2N 4N1, Canada.

D Corresponding author. Email: jpkastel@ucalgary.ca

Reproduction, Fertility and Development 31(4) 683-688 https://doi.org/10.1071/RD17509
Submitted: 1 December 2017  Accepted: 15 October 2018   Published: 19 November 2018

Abstract

There is a paradigm that testicular hyperthermia fails to increase testicular blood flow and that an ensuing hypoxia impairs spermatogenesis. However, in our previous studies, decreases in normal and motile spermatozoa after testicular warming were neither prevented by concurrent hyperoxia nor replicated by hypoxia. The objective of the present study was to determine the effects of increasing testicular temperature on testicular blood flow and O2 delivery and uptake and to detect evidence of anaerobic metabolism. Under general anaesthesia, the testicular temperature of nine crossbred rams was sequentially maintained at ~33°C, 37°C and 40°C (±0.5°C; 45 min per temperature). As testicular temperature increased from 33°C to 40°C there were increases in testicular blood flow (13.2 ± 2.7 vs 17.7 ± 3.2 mL min−1 per 100 g of testes, mean ± s.e.m.; P < 0.05), O2 extraction (31.2 ± 5.0 vs 47.3 ± 3.1%; P < 0.0001) and O2 consumption (0.35 ± 0.04 vs 0.64 ± 0.06 mL min−1 per 100 g of testes; P < 0.0001). There was no evidence of anaerobic metabolism, based on a lack of change in lactate, pH, HCO3 and base excess. In conclusion, these data challenge the paradigm regarding scrotal–testicular thermoregulation, as acute testicular hyperthermia increased blood flow and tended to increase O2 delivery and uptake, with no indication of hypoxia or anaerobic metabolism.

Additional keywords: testis, increased testicular temperature, scrotal–testicular thermoregulation, aerobic metabolism


References

Adeva-Andany, M., Lopez-Ojen, M., Funcasta-Calderon, R., Ameneiros-Rodriguez, E., Donapetry-Garcia, C., Vila-Altesor, M., and Rodriguez-Seijas, J. (2014). Comprehensive review on lactate metabolism in human health. Mitochondrion 17, 76–100.
Comprehensive review on lactate metabolism in human health.Crossref | GoogleScholarGoogle Scholar |

Barros Adwell, C. M. Q., Brito, L. F. C., Oba, E., Wilde, R. E., Rizzoto, G., Thundathil, J. C., and Kastelic, J. P. (2018). Arterial blood flow is the main source of testicular heat in bulls and higher ambient temperatures significantly increase testicular blood flow. Theriogenology 116, 12–16.
Arterial blood flow is the main source of testicular heat in bulls and higher ambient temperatures significantly increase testicular blood flow.Crossref | GoogleScholarGoogle Scholar |

Brito, L. F., Barth, A. D., Wilde, R. E., and Kastelic, J. P. (2012). Testicular vascular cone development and its association with scrotal temperature, semen quality, and sperm production in beef bulls. Anim. Reprod. Sci. 134, 135–140.
Testicular vascular cone development and its association with scrotal temperature, semen quality, and sperm production in beef bulls.Crossref | GoogleScholarGoogle Scholar |

Carlsson, C., Hägerdal, M., and Siesjö, B. K. (1976). The effect of hyperthermia upon oxygen consumption and upon organic phosphates, glycolytic metabolites, citric acid cycle intermediates and associated amino acids in rat cerebral cortex. J. Neurochem. 26, 1001–1006.
The effect of hyperthermia upon oxygen consumption and upon organic phosphates, glycolytic metabolites, citric acid cycle intermediates and associated amino acids in rat cerebral cortex.Crossref | GoogleScholarGoogle Scholar |

Caulkett, N. A., Duke, T., and Cribb, P. H. (1996). Cardiopulmonary effects of medetomidine: ketamine in domestic sheep (Ovis ovis) maintained in sternal recumbency. J. Zoo Wildl. Med. 27, 217–226.

Ceylan, C., Aydilek, N., and Ipek, H. (2007). Effects of tiletamine-zolazepam anaesthesia on plasma antioxidative status and some haematological parameters in sheep. Acta Vet. Hung. 55, 191–197.
Effects of tiletamine-zolazepam anaesthesia on plasma antioxidative status and some haematological parameters in sheep.Crossref | GoogleScholarGoogle Scholar |

Chang, A. J., Ortega, F. E., Riegler, J., Madison, D. V., and Krasnow, M. A. (2015). Oxygen regulation of breathing through an olfactory receptor activated by lactate. Nature 527, 240–244.
Oxygen regulation of breathing through an olfactory receptor activated by lactate.Crossref | GoogleScholarGoogle Scholar |

Drescher, U., Koschate, J., Hoffmann, U., Schneider, S., and Werner, A. (2018). Effect of acute ambient temperature exposure on cardio–pulmonary and respiratory kinetics in men. Int. J. Hyperthermia 34, 442–454.
Effect of acute ambient temperature exposure on cardio–pulmonary and respiratory kinetics in men.Crossref | GoogleScholarGoogle Scholar |

Freeman, S. (1990). The evolution of the scrotum: a new hypothesis. J. Theor. Biol. 145, 429–445.
The evolution of the scrotum: a new hypothesis.Crossref | GoogleScholarGoogle Scholar |

González-Alonso, J., Calbet, J. A. L., Boushel, R., Helge, J. W., Søndergaard, H., Munch-Andersen, T., van Hall, G., Mortensen, S. P., and Secher, N. H. (2015). Blood temperature and perfusion to exercising and non-exercising human limbs. Exp. Physiol. 100, 1118–1131.
Blood temperature and perfusion to exercising and non-exercising human limbs.Crossref | GoogleScholarGoogle Scholar |

Kastelic, J. P., Coulter, G. H., and Cook, R. B. (1995). Scrotal surface, subcutaneous, intratesticular, and intraepididymal temperatures in bulls. Theriogenology 44, 147–152.
Scrotal surface, subcutaneous, intratesticular, and intraepididymal temperatures in bulls.Crossref | GoogleScholarGoogle Scholar |

Kastelic, J. P., Wilde, R. E., Rizzoto, G., and Thundathil, J. C. (2017). Hyperthermia and not hypoxia may reduce sperm motility and morphology following testicular hyperthermia. Vet. Med. (Praha) 62, 437–442.
Hyperthermia and not hypoxia may reduce sperm motility and morphology following testicular hyperthermia.Crossref | GoogleScholarGoogle Scholar |

Lee, D. C., Sohn, H. A., Park, Z. Y., Oh, S., Kang, Y. K., Lee, K. M., Kang, M., Jang, Y. J., Yang, S. J., Hong, Y. K., Noh, H., Kim, J. A., Kim, D. J., Bae, K. H., Kim, D. M., Chung, S. J., Yoo, H. S., Yu, D. Y., Park, K. C., and Yeom, Y. I. (2015). A lactate-induced response to hypoxia. Cell 161, 595–609.
A lactate-induced response to hypoxia.Crossref | GoogleScholarGoogle Scholar |

Maloney, S. K., and Mitchell, D. (1996). Regulation of ram scrotal temperature during heat exposure, cold exposure, fever and exercise. J. Physiol. 496, 421–430.
Regulation of ram scrotal temperature during heat exposure, cold exposure, fever and exercise.Crossref | GoogleScholarGoogle Scholar |

Mieusset, R., Sowerbutts, S. F., Zupp, J. L., and Setchell, B. P. (1992). Increased flow of testicular blood plasma during local heating of the testes of rams. J. Reprod. Fertil. 94, 345–352.
Increased flow of testicular blood plasma during local heating of the testes of rams.Crossref | GoogleScholarGoogle Scholar |

Raekallio, M. R., Honkavaara, J. M., and Vainio, O. M. (2010). The effects of L-659,066, a peripheral α2-adrenoceptor antagonist, and verapamil on the cardiovascular influences of dexmedetomidine in conscious sheep. J. Vet. Pharmacol. Ther. 33, 434–438.
The effects of L-659,066, a peripheral α2-adrenoceptor antagonist, and verapamil on the cardiovascular influences of dexmedetomidine in conscious sheep.Crossref | GoogleScholarGoogle Scholar |

Schlünzen, L., Cold, G. E., Rasmussen, M., and Vafaee, M. S. (2006). Effects of dose-dependent levels of isoflurane on cerebral blood flow in healthy subjects studied using positron emission tomography. Acta Anaesthesiol. Scand. 50, 306–312.
Effects of dose-dependent levels of isoflurane on cerebral blood flow in healthy subjects studied using positron emission tomography.Crossref | GoogleScholarGoogle Scholar |

Schumacker, P. T., Long, G. R., and Wood, L. D. (1987). Tissue oxygen extraction during hypovolemia: role of hemoglobin P50. J. Appl. Physiol. 62, 1801–1807.
Tissue oxygen extraction during hypovolemia: role of hemoglobin P50.Crossref | GoogleScholarGoogle Scholar |

Semeniuk, L. M., Belenkie, I., and Tyberg, J. V. (1998). Acute effects of toborinone on vascular capacitance and conductance in experimental heart failure. Circulation 98, 58–63.
Acute effects of toborinone on vascular capacitance and conductance in experimental heart failure.Crossref | GoogleScholarGoogle Scholar |

Waites, G. M., and Setchell, B. P. (1964). Effect of local heating on blood flow and metabolism in the testis of the conscious ram. J. Reprod. Fertil. 8, 339–349.
Effect of local heating on blood flow and metabolism in the testis of the conscious ram.Crossref | GoogleScholarGoogle Scholar |

Wilson, D. V., Evans, A. T., Carpenter, E. R., and Mullineaux, D. R. (2004). The effect of four anesthetic protocols on splenic size in dogs. Vet. Anaesth. Analg. 31, 102–108.
The effect of four anesthetic protocols on splenic size in dogs.Crossref | GoogleScholarGoogle Scholar |