Diurnal rhythms in testicular blood flow, testicular morphometry and reproductive hormones in Shiba goats
Haney Samir
A B * , Ahmed S. Mandour C D , Faten Radwan B E , Ayman A. Swelum F , Tomohiko Yoshida D , Ryou Tanaka D , Kentaro Nagaoka B and Gen Watanabe B
+ Author Affiliations
- Author Affiliations
A Department of Theriogenology, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt.
B Laboratory of Veterinary Physiology, Department of Veterinary Medicine, Faculty of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-Cho, Fuchu, Tokyo 183-8509, Japan.
C Department of Animal Medicine (Internal Medicine), Faculty of Veterinary Medicine, Suez Canal University, Ismailia 41522, Egypt.
D Laboratory of Veterinary Surgery, Tokyo University of Agriculture and Technology, Tokyo 183-8509, Japan.
E Faculty of Veterinary Medicine, Benha University, Moshtohor, Toukh, Elqaliobiya 13736, Egypt.
F Department of Theriogenology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt.
Handling Editor: James Cummins
Reproduction, Fertility and Development 34(16) 1043-1051 https://doi.org/10.1071/RD22139
Published online: 4 October 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Testicular blood flow (TBF) is crucial for testicular function. The pattern of TBF in Shiba goats indicates seasonal variations.
Aims: This study aimed to investigate the effect of diurnal variations on TBF, testis volume (TV), testicular echogenicity, and reproductive hormones in goats over a 24-h period.
Methods: In three trials that went for three consecutive days each, 12 bucks were scanned using Triplex ultrasonography to assess the TV, pixel intensity of testicular echotexture (PIX), and Doppler indices of TBF (resistive index: RI and pulsatility index: PI) in four-time points a day (at 6.00, 12.00, 18.00, and 00.00 h). Concomitantly, the changes in circulating FSH, LH, inhibin, testosterone (T), estradiol (E2), cortisol, and melatonin were assessed.
Key results: Results revealed diurnal alterations in the calculated RI of TBF and the PIX of testicular parenchyma (P < 0.05). Lower RI values of the TBF were observed at 6.00 h compared to other time points. There were significant diurnal alterations in the levels of FSH (P < 0.05), LH (P < 0.05), T (P < 0.0001), E2 (P < 0.0001), cortisol (P < 0.0001), and melatonin (P < 0.0001). FSH attained a higher concentration at 18.00 h compared to 12.00 h. Concentrations of LH were significantly higher at 06.00 h compared to those at 18.00 h. Concentrations of T were significantly higher at 6.00 compared to other time points. E2 showed higher concentrations at 6.00 h and 00.00 h compared to 12.00 h and 18.00 h. On the contrary, concentrations of cortisol were significantly higher at 12.00 h and 18.00 h compared to 06.00 h and 00.00 h. The highest concentrations of melatonin were observed at 00.00 h compared to other time points, while the lowest concentrations were at 12.00 h.
Conclusions: Diurnal rhythm induces significant changes in TBF, testicular PIX, and circulating FSH, LH, T, E2, cortisol, and melatonin over the 24-h day.
Implications: The outcomes of the study are reflected in the advisability of monitoring the TBF at a fixed time a day to avoid the circadian rhythm effect.
Keywords: diurnal rhythm, goats, hormones, resistive index, testicular blood flow, testicular echogenicity, testis, triplex Doppler.
References
Ahmadi, B, Lau, CP-S, Giffin, J, Santos, N, Hahnel, A, Raeside, J, Christie, H, and Bartlewski, P (2012). Suitability of epididymal and testicular ultrasonography and computerized image analysis for assessment of current and future semen quality in the ram. Experimental Biology and Medicine 237, 186–193.| Suitability of epididymal and testicular ultrasonography and computerized image analysis for assessment of current and future semen quality in the ram.Crossref | GoogleScholarGoogle Scholar |
Angelousi, A, Kassi, E, Nasiri-Ansari, N, Weickert, MO, Randeva, H, and Kaltsas, G (2018). Clock genes alterations and endocrine disorders. European Journal of Clinical Investigation 48, e12927.
| Clock genes alterations and endocrine disorders.Crossref | GoogleScholarGoogle Scholar |
Arai, K, Watanabe, G, Fujimoto, M, Nagata, S, Takemura, Y, Taya, K, and Sasamoto, S (1995). A sensitive radioimmunoassay for cortisol using 125I-labeled radioligand. Journal of Reproduction and Development 41, j15–j20.
| A sensitive radioimmunoassay for cortisol using 125I-labeled radioligand.Crossref | GoogleScholarGoogle Scholar |
Araki, K, Arai, KY, Watanabe, G, and Taya, K (2000). Involvement of inhibin in the regulation of follicle-stimulating hormone secretion in the young adult male Shiba goat. Journal of Andrology 21, 558–565.
Bollwein, H, Schulze, JJ, Miyamoto, A, and Sieme, H (2008). Testicular blood flow and plasma concentrations of testosterone and total estrogen in the stallion after the administration of human chorionic gonadotropin. Journal of Reproduction and Development 54, 335–339.
| Testicular blood flow and plasma concentrations of testosterone and total estrogen in the stallion after the administration of human chorionic gonadotropin.Crossref | GoogleScholarGoogle Scholar |
Brambilla, DJ, Matsumoto, AM, Araujo, AB, and McKinlay, JB (2009). The effect of diurnal variation on clinical measurement of serum testosterone and other sex hormone levels in men. The Journal of Clinical Endocrinology & Metabolism 94, 907–913.
| The effect of diurnal variation on clinical measurement of serum testosterone and other sex hormone levels in men.Crossref | GoogleScholarGoogle Scholar |
Bray, MS, and Young, ME (2008). Diurnal variations in myocardial metabolism. Cardiovascular Research 79, 228–237.
| Diurnal variations in myocardial metabolism.Crossref | GoogleScholarGoogle Scholar |
Brito, LFC, Silva, AEDF, Rodrigues, LH, Vieira, FV, Deragon, LAG, and Kastelic, JP (2002). Effect of age and genetic group on characteristics of the scrotum, testes and testicular vascular cones, and on sperm production and semen quality in AI bulls in Brazil. Theriogenology 58, 1175–1186.
| Effect of age and genetic group on characteristics of the scrotum, testes and testicular vascular cones, and on sperm production and semen quality in AI bulls in Brazil.Crossref | GoogleScholarGoogle Scholar |
Brito, LFC, Barth, AD, Wilde, RE, and Kastelic, JP (2012). Testicular ultrasonogram pixel intensity during sexual development and its relationship with semen quality, sperm production, and quantitative testicular histology in beef bulls. Theriogenology 78, 69–76.
| Testicular ultrasonogram pixel intensity during sexual development and its relationship with semen quality, sperm production, and quantitative testicular histology in beef bulls.Crossref | GoogleScholarGoogle Scholar |
Camela, ESC, Nociti, RP, Santos, VJC, Macente, BI, Murawski, M, Vicente, WRR, Bartlewski, PM, and Oliveira, MEF (2019). Changes in testicular size, echotexture, and arterial blood flow associated with the attainment of puberty in Dorper rams raised in a subtropical climate. Reproduction in Domestic Animals 54, 131–137.
| Changes in testicular size, echotexture, and arterial blood flow associated with the attainment of puberty in Dorper rams raised in a subtropical climate.Crossref | GoogleScholarGoogle Scholar |
Casao, A, Gallego, M, Abecia, JA, Forcada, F, Pérez-Pé, R, Muiño-Blanco, T, and Cebrián-Pérez, JÁ (2012). Identification and immunolocalisation of melatonin MT1 and MT2 receptors in Rasa Aragonesa ram spermatozoa. Reproduction, Fertility and Development 24, 953–961.
| Identification and immunolocalisation of melatonin MT1 and MT2 receptors in Rasa Aragonesa ram spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Chen, H, Gao, L, Xiong, Y, Yang, D, Li, C, Wang, A, and Jin, Y (2017). Circadian clock and steroidogenic-related gene expression profiles in mouse Leydig cells following dexamethasone stimulation. Biochemical and Biophysical Research Communications 483, 294–300.
| Circadian clock and steroidogenic-related gene expression profiles in mouse Leydig cells following dexamethasone stimulation.Crossref | GoogleScholarGoogle Scholar |
Edgar, RS, Green, EW, Zhao, Y, van Ooijen, G, Olmedo, M, Qin, X, Xu, Y, Pan, M, Valekunja, UK, Feeney, KA, Maywood, ES, Hastings, MH, Baliga, NS, Merrow, M, Millar, AJ, Johnson, CH, Kyriacou, CP, O’Neill, JS, and Reddy, AB (2012). Peroxiredoxins are conserved markers of circadian rhythms. Nature 485, 459–464.
| Peroxiredoxins are conserved markers of circadian rhythms.Crossref | GoogleScholarGoogle Scholar |
El-Sherbiny, HR, El-Shalofy, AS, and Samir, H (2022a). Exogenous L-carnitine administration ameliorates the adverse effects of heat stress on testicular hemodynamics, echotexture, and total antioxidant capacity in rams. Frontiers in Veterinary Science 9, 860771.
| Exogenous L-carnitine administration ameliorates the adverse effects of heat stress on testicular hemodynamics, echotexture, and total antioxidant capacity in rams.Crossref | GoogleScholarGoogle Scholar |
El-Sherbiny, HR, Fathi, M, Samir, H, and Abdelnaby, EA (2022b). Supplemental dietary curcumin improves testicular hemodynamics, testosterone levels, and semen quality in Baladi bucks in the non-breeding season. Theriogenology 188, 100–107.
| Supplemental dietary curcumin improves testicular hemodynamics, testosterone levels, and semen quality in Baladi bucks in the non-breeding season.Crossref | GoogleScholarGoogle Scholar |
El-Sherbiny, HR, Samir, H, El-Shalofy, AS, and Abdelnaby, EA (2022c). Exogenous L-arginine administration improves uterine vascular perfusion, uteroplacental thickness, steroid concentrations and nitric oxide levels in pregnant buffaloes under subtropical conditions. Reproduction in Domestic Animals , .
| Exogenous L-arginine administration improves uterine vascular perfusion, uteroplacental thickness, steroid concentrations and nitric oxide levels in pregnant buffaloes under subtropical conditions.Crossref | GoogleScholarGoogle Scholar |
Faiman, C, and Winter, JSD (1971). Diurnal cycles in plasma FSH, testosterone and cortisol in men. The Journal of Clinical Endocrinology & Metabolism 33, 186–192.
| Diurnal cycles in plasma FSH, testosterone and cortisol in men.Crossref | GoogleScholarGoogle Scholar |
Ferlazzo, N, Andolina, G, Cannata, A, Costanzo, MG, Rizzo, V, Currò, M, Ientile, R, and Caccamo, D (2020). Is melatonin the cornucopia of the 21st century? Antioxidants 9, 1088.
| Is melatonin the cornucopia of the 21st century?Crossref | GoogleScholarGoogle Scholar |
Frungieri, MB, Calandra, RS, and Rossi, SP (2017). Local actions of melatonin in somatic cells of the testis. International Journal of Molecular Sciences 18, 1170.
| Local actions of melatonin in somatic cells of the testis.Crossref | GoogleScholarGoogle Scholar |
Gamble, KL, Berry, R, Frank, SJ, and Young, ME (2014). Circadian clock control of endocrine factors. Nature Reviews Endocrinology 10, 466–475.
| Circadian clock control of endocrine factors.Crossref | GoogleScholarGoogle Scholar |
Giannetto, C, Carcangiu, V, Luridiana, S, Parmeggiani, A, and Piccione, G (2020). Twenty-four-hour rhythm patterns of plasma melatonin in short-day and long-day breeders maintained under natural environmental conditions. Chronobiology International 37, 974–979.
| Twenty-four-hour rhythm patterns of plasma melatonin in short-day and long-day breeders maintained under natural environmental conditions.Crossref | GoogleScholarGoogle Scholar |
Ginther, OJ, Utt, MD, and Beg, MA (2007). Follicle deviation and diurnal variation in circulating hormone concentrations in mares. Animal Reproduction Science 100, 197–203.
| Follicle deviation and diurnal variation in circulating hormone concentrations in mares.Crossref | GoogleScholarGoogle Scholar |
Hamada, T, Watanabe, G, Kokuho, T, Taya, K, Sasamoto, S, Hasegawa, Y, Miyamoto, K, and Igarashi, M (1989). Radioimmunoassay of inhibin in various mammals. Journal of Endocrinology 122, 697–704.
| Radioimmunoassay of inhibin in various mammals.Crossref | GoogleScholarGoogle Scholar |
Hannan, MA, Fuenzalida, MJ, Siddiqui, MAR, Shamsuddin, M, Beg, MA, and Ginther, OJ (2010). Diurnal variation in LH and temporal relationships between oscillations in LH and progesterone during the luteal phase in heifers. Theriogenology 74, 1491–1498.
| Diurnal variation in LH and temporal relationships between oscillations in LH and progesterone during the luteal phase in heifers.Crossref | GoogleScholarGoogle Scholar |
Hedia, M, and El-Shalofy, A (2022). Ageing affects plasma steroid concentrations and testicular volume, echotexture and haemodynamics in rams. Andrologia 54, e14309.
| Ageing affects plasma steroid concentrations and testicular volume, echotexture and haemodynamics in rams.Crossref | GoogleScholarGoogle Scholar |
Junior, FAB, Junior, CK, Fávaro, PC, Pereira, GR, Morotti, F, Menegassi, SRO, Barcellos, JOJ, and Seneda, MM (2018). Effect of breed on testicular blood flow dynamics in bulls. Theriogenology 118, 16–21.
| Effect of breed on testicular blood flow dynamics in bulls.Crossref | GoogleScholarGoogle Scholar |
Kinson, GA, and Liu, C-C (1973). Diurnal variation in plasma testosterone of the male laboratory rat. Hormone and Metabolic Research 5, 233–234.
| Diurnal variation in plasma testosterone of the male laboratory rat.Crossref | GoogleScholarGoogle Scholar |
Larsen, GD (2015). A reliable ruminate for research. Lab Animal 44, 337.
| A reliable ruminate for research.Crossref | GoogleScholarGoogle Scholar |
Lemley, CO, Meyer, AM, Camacho, LE, Neville, TL, Newman, DJ, Caton, JS, and Vonnahme, KA (2012). Melatonin supplementation alters uteroplacental hemodynamics and fetal development in an ovine model of intrauterine growth restriction. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 302, R454–R467.
| Melatonin supplementation alters uteroplacental hemodynamics and fetal development in an ovine model of intrauterine growth restriction.Crossref | GoogleScholarGoogle Scholar |
Mandour, AS, Mahmoud, AE, Ali, AO, Matsuura, K, Samir, H, Abdelmageed, HA, Ma, D, Yoshida, T, Hamabe, L, Uemura, A, Watanabe, G, and Tanaka, R (2021). Expression of cardiac copper chaperone encoding genes and their correlation with cardiac function parameters in goats. Veterinary Research Communications 45, 305–317.
| Expression of cardiac copper chaperone encoding genes and their correlation with cardiac function parameters in goats.Crossref | GoogleScholarGoogle Scholar |
Mandour, AS, Samir, H, Yoshida, T, Matsuura, K, Hamabe, L, Shimada, K, Elbadawy, M, Uemura, A, Abdelmageed, H, Takahashi, K, Watanabe, G, and Tanaka, R (2022). Novel color-M mode echocardiography for non-invasive assessment of the intraventricular pressure in goats: feasibility, repeatability, and the effect of sedation. Frontiers in Veterinary Science , .
| Novel color-M mode echocardiography for non-invasive assessment of the intraventricular pressure in goats: feasibility, repeatability, and the effect of sedation.Crossref | GoogleScholarGoogle Scholar |
Mesbah, S, and Brudieux, R (1982). Diurnal variation of plasma concentrations of cortisol, aldosterone and electrolytes in the ram. Hormone and Metabolic Research 14, 320–323.
| Diurnal variation of plasma concentrations of cortisol, aldosterone and electrolytes in the ram.Crossref | GoogleScholarGoogle Scholar |
Mori, Y, and Kano, Y (1984). Changes in plasma concentrations of LH, progesterone and oestradiol in relation to the occurrence of luteolysis, oestrus and time of ovulation in the Shiba goat (Capra hircus). Reproduction 72, 223–230.
| Changes in plasma concentrations of LH, progesterone and oestradiol in relation to the occurrence of luteolysis, oestrus and time of ovulation in the Shiba goat (Capra hircus).Crossref | GoogleScholarGoogle Scholar |
Ntemka, A, Kiossis, E, Boscos, C, Theodoridis, A, Kourousekos, G, and Tsakmakidis, I (2018). Effects of testicular hemodynamic and echogenicity changes on ram semen characteristics. Reproduction in Domestic Animals 53, 50–55.
| Effects of testicular hemodynamic and echogenicity changes on ram semen characteristics.Crossref | GoogleScholarGoogle Scholar |
Odawara, H, Iwasaki, T, Horiguchi, J, Rokutanda, N, Hirooka, K, Miyazaki, W, Koibuchi, Y, Shimokawa, N, Iino, Y, Takeyoshi, I, and Koibuchi, N (2009). Activation of aromatase expression by retinoic acid receptor-related orphan receptor (ROR) α in breast cancer cells: identification of a novel ROR response element. Journal of Biological Chemistry 284, 17711–17719.
| Activation of aromatase expression by retinoic acid receptor-related orphan receptor (ROR) α in breast cancer cells: identification of a novel ROR response element.Crossref | GoogleScholarGoogle Scholar |
Paltiel, HJ, Diamond, DA, Di Canzio, J, Zurakowski, D, Borer, JG, and Atala, A (2002). Testicular volume: comparison of orchidometer and US measurements in dogs. Radiology 222, 114–119.
| Testicular volume: comparison of orchidometer and US measurements in dogs.Crossref | GoogleScholarGoogle Scholar |
Pandi-Perumal, SR, Trakht, I, Srinivasan, V, Spence, DW, Maestroni, GJ, Zisapel, N, and Cardinali, DP (2008). Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways. Progress in Neurobiology 85, 335–353.
| Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways.Crossref | GoogleScholarGoogle Scholar |
Panico, S, Pisani, P, Muti, P, Recchione, C, Cavalleri, A, Totis, A, and Berrino, F (1990). Diurnal variation of testosterone and estradiol: a source of bias in comparative studies on breast cancer. Journal of Endocrinological Investigation 13, 423–426.
| Diurnal variation of testosterone and estradiol: a source of bias in comparative studies on breast cancer.Crossref | GoogleScholarGoogle Scholar |
Paulis, L, and Simko, F (2007). Blood pressure modulation and cardiovascular protection by melatonin: potential mechanisms behind. Physiological Research 56, 671–684.
| Blood pressure modulation and cardiovascular protection by melatonin: potential mechanisms behind.Crossref | GoogleScholarGoogle Scholar |
Pozor, M, Morrissey, H, Albanese, V, Khouzam, N, Deriberprey, A, Macpherson, ML, and Kelleman, AA (2017). Relationship between echotextural and histomorphometric characteristics of stallion testes. Theriogenology 99, 134–145.
| Relationship between echotextural and histomorphometric characteristics of stallion testes.Crossref | GoogleScholarGoogle Scholar |
Rosenfeld, CR, Roy, T, and Cox, BE (2002). Mechanisms modulating estrogen-induced uterine vasodilation. Vascular Pharmacology 38, 115–125.
| Mechanisms modulating estrogen-induced uterine vasodilation.Crossref | GoogleScholarGoogle Scholar |
Rüger, M, and Scheer, FAJL (2009). Effects of circadian disruption on the cardiometabolic system. Reviews in Endocrine and Metabolic Disorders 10, 245–260.
| Effects of circadian disruption on the cardiometabolic system.Crossref | GoogleScholarGoogle Scholar |
Samir, H, Sasaki, K, Ahmed, E, Karen, A, Nagaoka, K, El Sayed, M, Taya, K, and Watanabe, G (2015). Effect of a single injection of gonadotropin-releasing hormone (GnRH) and human chorionic gonadotropin (hCG) on testicular blood flow measured by color doppler ultrasonography in male Shiba goats. Journal of Veterinary Medical Science 77, 549–556.
| Effect of a single injection of gonadotropin-releasing hormone (GnRH) and human chorionic gonadotropin (hCG) on testicular blood flow measured by color doppler ultrasonography in male Shiba goats.Crossref | GoogleScholarGoogle Scholar |
Samir, H, Nyametease, P, Nagaoka, K, and Watanabe, G (2018). Effect of seasonality on testicular blood flow as determined by color Doppler ultrasonography and hormonal profiles in Shiba goats. Animal Reproduction Science 197, 185–192.
| Effect of seasonality on testicular blood flow as determined by color Doppler ultrasonography and hormonal profiles in Shiba goats.Crossref | GoogleScholarGoogle Scholar |
Samir, H, Nyametease, P, Elbadawy, M, Nagaoka, K, Sasaki, K, and Watanabe, G (2020a). Administration of melatonin improves testicular blood flow, circulating hormones, and semen quality in Shiba goats. Theriogenology 146, 111–119.
| Administration of melatonin improves testicular blood flow, circulating hormones, and semen quality in Shiba goats.Crossref | GoogleScholarGoogle Scholar |
Samir, H, El Sayed, MAI, Nagaoka, K, Sasaki, K, Abo El-Maaty, AM, Karen, A, Abou-Ahmed, MM, and Watanabe, G (2020b). Passive immunization against inhibin increases testicular blood flow in male goats. Theriogenology 147, 85–91.
| Passive immunization against inhibin increases testicular blood flow in male goats.Crossref | GoogleScholarGoogle Scholar |
Samir, H, Radwan, F, and Watanabe, G (2021). Advances in applications of color Doppler ultrasonography in the andrological assessment of domestic animals: a review. Theriogenology 161, 252–261.
| Advances in applications of color Doppler ultrasonography in the andrological assessment of domestic animals: a review.Crossref | GoogleScholarGoogle Scholar |
Sayegh, JF, Kobor, G, Lajtha, A, and Vadasz, C (1990). Effects of social isolation and the time of day on testosterone levels in plasma of C57BL/6By and BALB/cBy mice. Steroids 55, 79–82.
| Effects of social isolation and the time of day on testosterone levels in plasma of C57BL/6By and BALB/cBy mice.Crossref | GoogleScholarGoogle Scholar |
Taya, K, Watanabe, G, and Sasamoto, S (1985). Radioimmunoassay for progesterone, testosterone and estradiol-17β using 125I-Iodohistamine radioligands. The Japanese Journal of Animal Reproduction 31, 186–197.
| Radioimmunoassay for progesterone, testosterone and estradiol-17β using 125I-Iodohistamine radioligands.Crossref | GoogleScholarGoogle Scholar |
Thakor, AS, Herrera, EA, Serón-Ferré, M, and Giussani, DA (2010). Melatonin and vitamin C increase umbilical blood flow via nitric oxide-dependent mechanisms. Journal of Pineal Research 49, 399–406.
| Melatonin and vitamin C increase umbilical blood flow via nitric oxide-dependent mechanisms.Crossref | GoogleScholarGoogle Scholar |
Tomlinson, M, Jennings, A, Macrae, A, and Truyers, I (2017). The value of trans-scrotal ultrasonography at bull breeding soundness evaluation (BBSE): the relationship between testicular parenchymal pixel intensity and semen quality. Theriogenology 89, 169–177.
| The value of trans-scrotal ultrasonography at bull breeding soundness evaluation (BBSE): the relationship between testicular parenchymal pixel intensity and semen quality.Crossref | GoogleScholarGoogle Scholar |
Xie, Y, Tang, Q, Chen, G, Xie, M, Yu, S, Zhao, J, and Chen, L (2019). New insights into the circadian rhythm and its related diseases. Frontiers in Physiology 10, 682.
| New insights into the circadian rhythm and its related diseases.Crossref | GoogleScholarGoogle Scholar |
