Evaluation of Placentome Perfusion in Goats with Pregnancy Toxemia

Öz

The aim of the presented study was to determine the effects of pregnancy toxemia (PT) on placental blood flow in goats. The control group (n=15) consisted of goats with β-hydroxybutyric acid (BHBA) concentrations <0.8 mmol/L, the subclinical PT group (n=15) consisted of goats with BHBA concentrations between 0.8 and 1.6 mmol/L, and the clinical PT group (n=15) consisted of goats with BHBA concentrations between 1.6 and 5 mmol/L. Before any treatment or administration, caruncle and cotyledonary arteries were evaluated by Pulse Doppler ultrasonography (USG) in all goats. In addition, non-esterified fatty acid (NEFA) and nitric oxide (NO) concentrations were analyzed using commercial kits, and glucose levels were analyzed with a biochemistry device. Nitric oxide, BHBA and NEFA concentrations were lowest in the control group and highest in the clinical PT group (P<0.001). Glucose concentration was lowest in the clinical PT group and highest in the control group (P<0.001). Significant differences were observed between the groups in terms of PI, RI, PSV, EDV, and A values of the caruncle and cotyledonary arteries (P<0.001). PI and RI values were highest in the control group and lowest in the clinical PT group (P<0.001); while PSV, EDV, and A values were lowest in the control group and highest in the clinical PT group (P<0.001). In conclusion, it was determined that pregnancy toxemia in goats causes significant changes in placental blood flow, and Doppler ultrasonography parameters may be a valuable tool in diagnosing the disease in goats during the late stages of pregnancy.

Anahtar Kelimeler

• Doppler;
• Goat
• Nitric Oxide;
• Pregnancy Toxemia

Etik Beyan

This study was carried out in accordance with the permission given by the Harran University Animal Experiments Local Ethics Committee (HRÜ-HADYEK) with the decision number 2025/001/07.

Gebelik Toksemisi Olan Keçilerde Plasentom Perfüzyonunun Değerlendirilmesi

Öz

Sunulan çalışmanın amacı, keçilerde gebelik toksemisinin (PT) plasental kan akımı üzerindeki etkilerini belirlemektir. Kontrol grubu (n=15), β-hidroksibütirik asit (BHBA) konsantrasyonu <0.8 mmol/L olan keçilerden; subklinik PT grubu (n=15), BHBA konsantrasyonu 0.8–1.6 mmol/L arasında olan keçilerden; klinik PT grubu (n=15) ise BHBA konsantrasyonu 1.6–5 mmol/L arasında olan keçilerden oluşturuldu. Herhangi bir tedavi veya uygulama öncesinde, tüm keçilerde karunkular ve kotiledoner arterler Pulse Doppler ultrasonografi (USG) ile değerlendirildi. Ayrıca, non-esterifiye yağ asidi (NEFA) ve nitrik oksit (NO) konsantrasyonları ticari kitler kullanılarak analiz edildi ve glukoz düzeyleri biyokimya cihazı ile ölçüldü. Nitrik oksit, BHBA ve NEFA konsantrasyonlarının en düşük kontrol grubunda, en yüksek ise klinik PT grubunda olduğu belirl grubunda bulundu. (P<0.001). Karunkular ve kotiledoner arterlere ait PI, RI, PSV, EDV ve A parametreleri açısından gruplar arasında anlamlı farklılıklar gözlendi (P<0.001). PI ve RI değerleri en yüksek kontrol grubunda, en düşük klinik PT grubunda belirlenirken (P<0.001); PSV, EDV ve A değerleri en düşük kontrol grubunda, en yüksek klinik PT grubunda belirlendi (P<0.001). Sonuç olarak, keçilerde gebelik toksemisinin plasental kan akımında önemli değişikliklere yol açtığı ve Doppler ultrasonografi parametrelerinin gebeliğin ileri dönemlerinde hastalığın tanısında değerli bir araç olabileceği belirlendi.

Anahtar Kelimeler

• Doppler
• Gebelik Toksemisi;
• Keçi;
• Nitrik Oksit

Etik Beyan

Bu çalışma, Harran Üniversitesi Hayvan Deneyleri Yerel Etik Kurulu'nun (HRÜ-HADYEK) 2025/001/07 numaralı kararıyla verilen izin doğrultusunda gerçekleştirilmiştir.

Kaynakça

1. Abdelaal, A., Zaher, H., Elgaml, S. A., & Abdallah, H. (2013). Prognostic value of serum cardiac troponin t and nitric oxide as cardiac biomarkers in pregnancy toxemic goats. Global Veterinaria Journal, 11(6), 817-823. doi: 10.5829/idosi.gv.2013.11.6.82261
2. Acharya, G., Sitras, V., Erkinaro, T., Mäkikallio, K., Kavasmaa, T., Päkkilä, M., Huhta, J.C. & Räsänen, J. (2007). Experimental validation of uterine artery volume blood flow measurement by Doppler ultrasonography in pregnant sheep. Ultrasound in Obstetrics and Gynecology: The Official Journal of the International Society of Ultrasound in Obstetrics and Gynecology, 29(4), 401-406. doi: https://doi.org/10.1002/uog.3977
3. Akkuş, T., & Yaprakci, Ö. (2024). The effect of pregnancy toxemia on serum carnitine and amino acid levels in goats. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 76(06), e13216. doi: https://doi.org/10.1590/1678-4162-13216
4. Akkuş, T., Emre, B., & Yaprakcı, Ö. (2023). Doppler Ultrasonography Assessment of Uterine Artery Blood Flow Throughout Late Pregnancy in Awassi Ewes. Animal Health Production and Hygiene, 12(2), 42-49. doi: https://doi.org/10.53913/aduveterinary.1326273
5. Andrews, A. (1997). Pregnancy toxaemia in the ewe. In Practice, 19(6), 306-314. doi: https://doi.org/10.1136/inpract.19.6.306
6. Barbagianni, M. S., Mavrogianni, V. S., Katsafadou, A. I., Spanos, S. A., Tsioli, V., Galatos, A. D., Nakou M, Valasi I, Gouletsou PG & Fthenakis, G. C. (2015). Pregnancy toxaemia as predisposing factor for development of mastitis in sheep during the immediately post-partum period. Small Ruminant Research, 130, 246-251. doi: https://doi.org/10.1016/j.smallrumres.2015.07.002
7. Brzozowska, A., Stankiewicz, T., Błaszczyk, B., Chundekkad, P., Udała, J., & Wojtasiak, N. (2022). Ultrasound parameters of early pregnancy and Doppler indices of blood vessels in the placenta and umbilical cord throughout the pregnancy period in sheep. BMC Veterinary Research, 18(1), 326. doi: https://doi.org/10.1186/s12917-022-03424-z
8. Camacho, L. E., Lemley, C. O., Dorsam, S. T., Swanson, K. C., & Vonnahme, K. A. (2018). Effects of maternal nutrient restriction followed by realimentation during early and mid-gestation in beef cows. II. Placental development, umbilical blood flow, and uterine blood flow responses to diet alterations. Theriogenology, 116, 1-11. doi: https://doi.org/10.1016/j.theriogenology.2018.04.013

9. Duehlmeier, R., Fluegge, I., Schwert, B., & Ganter, M. (2013). Post‐glucose load changes of plasma key metabolite and insulin concentrations during pregnancy and lactation in ewes with different susceptibility to pregnancy toxaemia. Journal of Animal Physiology and Animal Nutrition, 97(5), 971-985. doi: https://doi.org/10.1111/jpn.12010
10. Dusse, L. M. S. A., Silva, R. M. M. E., Vieira, L. M., & das Graças Carvalho, M. (2005). Does plasma nitrite determination by the Griess reaction reflect nitric oxide synthesis?. Clinica Chimica Acta; International Journal of Clinical Chemistry, 362(1-2), 195-197. doi: 10.1016/j.cccn.2005.06.007
11. Gagioti, S., Scavone, C., & Bevilacqua, E. (2000). Participation of the mouse implanting trophoblast in nitric oxide production during pregnancy. Biology of Reproduction, 62(2), 260-268. doi: https://doi.org/10.1095/biolreprod62.2.260
12. Hafez, S. A., Borowicz, P., Reynolds, L. P., & Redmer, D. A. (2010). Maternal and fetal microvasculature in sheep placenta at several stages of gestation. Journal of Anatomy, 216(3), 292-300. doi: https://doi.org/10.1111/j.1469-7580.2009.01184.x
13. Huang, L. T., Hsieh, C. S., Chang, K. A., & Tain, Y. L. (2012). Roles of nitric oxide and asymmetric dimethylarginine in pregnancy and fetal programming. International Journal of Molecular Sciences, 13(11), 14606-14622. doi: https://doi.org/10.3390/ijms131114606
14. Ji, X., Liu, N., Wang, Y., Ding, K., Huang, S., & Zhang, C. (2023). Pregnancy toxemia in ewes: A review of molecular metabolic mechanisms and management strategies. Metabolites, 13(2), 149. doi: https://doi.org/10.3390/metabo13020149
15. Kanjanaruch, C., Bochantin, K. A., Dávila Ruiz, B. J., Syring, J., Entzie, Y., King, L., Browicz PP, Crouse MS, Caton JS, Dahlen CR, Ward AK., & Reynolds, L. P. (2024). One-carbon metabolite supplementation to nutrient-restricted beef heifers affects placental vascularity during early pregnancy. Journal of Animal Science, 102, 44. doi: https://doi.org/10.1093/jas/skae044
16. Kemp, M. W., Musk, G. C., & Saito, M. (2013). Animal models for the study of infection-associated preterm birth. In Animal models for the study of human disease (pp. 863-888). Academic Press. doi: https://doi.org/10.1016/B978-0-12-415894-8.00035-X
17. Kivrak, M. B., Turk, S., Takci, A., Bolukbas, B., Agaoglu, R. T., & Coskun, A. (2023). Pulse wave Doppler ultrasound of umbilical cord in experimentally induced pregnancy toxemia in sheep. Research in Veterinary Science, 160, 18-25. doi: https://doi.org/10.1016/j.rvsc.2023.05.004
18. Kolb, H., Kempf, K., Röhling, M., Lenzen-Schulte, M., Schloot, N. C., & Martin, S. (2021). Ketone bodies: from enemy to friend and guardian angel. BMC Medicine, 19(1), 313. doi: https://doi.org/10.1186/s12916-021-02185-0
19. Lemley, C. O., Hart, C. G., Lemire, R. L., King, E. H., Hopper, R. M., Park, S. B., Rude BJ., & Burnett, D. D. (2018). Maternal nutrient restriction alters uterine artery hemodynamics and placentome vascular density in Bos indicus and Bos taurus. Journal of Animal Science, 96(11), 4823-4834. doi: https://doi.org/10.1093/jas/sky329
20. Lemley, C. O., Meyer, A. M., Camacho, L. E., Neville, T. L., Newman, D. J., Caton, J. S., & Vonnahme, K. A. (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(4), R454-R467. doi: https://doi.org/10.1152/ajpregu.00407.2011
21. Lima, M. S., Pascoal, R. A., Stilwell, G. T., & Hjerpe, C. A. (2012). Clinical findings, blood chemistry values, and epidemiologic data from dairy goats with pregnancy toxemia. The Bovine Practitioner, 102-110. doi: https://doi.org/10.21423/bovine-vol46no2p102-110
22. Lorenz, M. D., Coates, J. R., & Kent, M. (2011). Systemic or multifocal signs. Handbook of Veterinary Neurology, 432. doi: 10.1016/B978-1-4377-0651-2.10015-3
23. Ramírez-González, D., Poto, Á., Peinado, B., Almela, L., Navarro-Serna, S., & Ruiz, S. (2023). Ultrasonography of pregnancy in Murciano-Granadina goat breed: fetal growth indices and umbilical artery doppler parameters. Animals, 13(4), 618. doi: https://doi.org/10.3390/ani13040618
24. Reynolds, L. P., & Redmer, D. A. (2001). Angiogenesis in the placenta. Biology of Reproduction, 64(4), 1033-1040. doi: https://doi.org/10.1095/biolreprod64.4.1033
25. Reynolds, L. P., Borowicz, P. P., Caton, J. S., Vonnahme, K. A., Luther, J. S., Buchanan, D. S., Hafez SA, Grazul-Biliska AT., & Redmer, D. A. (2010). Uteroplacental vascular development and placental function: an update. International Journal of Developmental Biology, 54(2), 355. doi: 10.1387/ijdb.082799lr
26. Rook, J. S. (2000). Pregnancy toxemia of ewes, does, and beef cows. Veterinary Clinics of North America: Food Animal Practice, 16(2), 293-317. doi: https://doi.org/10.1016/S0749-0720(15)30107-9
27. Sammin, D., Markey, B., Bassett, H., & Buxton, D. (2009). The ovine placenta and placentitis—A review. Veterinary Microbiology, 135(1-2), 90-97. doi: https://doi.org/10.1016/j.vetmic.2008.09.054
28. Saw, S. N., Tay, J. J. H., Poh, Y. W., Yang, L., Tan, W. C., Tan, L. K., Clark A, Biswas A, Mattar CNZ., & Yap, C. H. (2018). Altered placental chorionic arterial biomechanical properties during intrauterine growth restriction. Scientific Reports, 8(1), 16526. doi: https://doi.org/10.1038/s41598-018-34834-5
29. Sawalha, R. M., Conington, J., Brotherstone, S., & Villanueva, B. (2007). Analyses of lamb survival of Scottish Blackface sheep. Animal, 1(1), 151-157. doi: 10.1017/S1751731107340056
30. Simpson, K. M., Taylor, J. D., & Streeter, R. N. (2019). Evaluation of prognostic indicators for goats with pregnancy toxemia. Journal of the American Veterinary Medical Association, 254(7), 859-867. doi: https://doi.org/10.2460/javma.254.7.859
31. Singh, R. A. J. I. V., Singh, A., Beigh, S. A., Sharma, N., & Singh, V. (2022). Effect of physiological status and parity on metabolic and trace element profile of crossbred Rambouillet sheep of Himalayan region. Tropical Animal Health and Production, 54(1), 63. doi: https://doi.org/10.1007/s11250-022-03068-z
32. Stankiewicz, T., Błaszczyk, B., Udała, J., & Chundekkad, P. (2020). Morphometric measurements of the umbilical cord and placentomes and Doppler parameters of the umbilical artery through ultrasonographic analysis in pregnant sheep. Small Ruminant Research, 184, 106043. doi: https://doi.org/10.1016/j.smallrumres.2019.106043
33. Tanner, A. R., Kennedy, V. C., Lynch, C. S., Hord, T. K., Winger, Q. A., Rozance, P. J., & Anthony, R. V. (2022). In vivo investigation of ruminant placenta function and physiology—a review. Journal of Animal Science, 100(6), skac045. doi: https://doi.org/10.1093/jas/skac045
34. Thompson, J. M., & Meyer, H. H. (1994). Body condition scoring of sheep. http://hdl.handle.net/1957/14303 Vasava, P. R., Jani, R. G., Goswami, H. V., Rathwa, S. D., & Tandel, F. B. (2016). Studies on clinical signs and biochemical alteration in pregnancy toxemic goats. Veterinary World, 9(8), 869. doi: 10.14202/vetworld.2016.869-874
35. Weaver, L. F., Boileau, M. J., Gilliam, L. L., & Taylor, J. D. (2021). Characterization of short-and long-term morbidity and mortality of goat kids born to does with pregnancy toxemia. Journal of Veterinary Internal Medicine, 35(2), 1155-1163. doi: https://doi.org/10.1111/jvim.16069
36. Wu, G., Bazer, F. W., Wallace, J. M., & Spencer, T. E. (2006). Board-invited review: intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science, 84(9), 2316-2337. doi: https://doi.org/10.2527/jas.2006-156
37. Yaprakci, Ö., Akkuş, T., & Emre, B. (2025). Investigation of the clinical effects of isoxsuprine hydrochloride administered before cesarean section in sheep on mother and newborn. Research in Veterinary Science, 188, 105610. doi: https://doi.org/10.1016/j.rvsc.2025.105610 Yaprakci, O., & Akkus, T. α-Klotho in Pregnancy Toxemia in Goats: A New Biomarker Candidate?. doi: 10.63673/EurasianJVetSci.458 Zullino, S., Buzzella, F., & Simoncini, T. (2018). Nitric oxide and the biology of pregnancy. Vascular Pharmacology, 110, 71-74. doi: https://doi.org/10.1016/j.vph.2018.07.004