Süt Sığırlarında Geçiş Dönemi Metabolik Profil ile Üreme Performansı ve Metabolik Rahatsızlıklar Arasındaki İlişkiler

Abstract

Süt sığırlarında laktasyon döngüsü; gebeliğin son evresinden yüksek süt sentezi ve sekresyonunun başladığı sürece geçiş yaparken önemli fizyolojik, besinsel, metabolik ve immünolojik değişimlere sahne olmaktadır. Doğum öncesi 3 hafta ile doğum sonrası 3-4 haftalık süreci kapsayan geçiş dönemi süt verimi, genel sağlık durumu ve üreme performansının belirlendiği en kritik aşamadır. Bu süreçte inekler, artan enerji gereksinimi ve azalan kuru madde tüketimi nedeniyle negatif enerji dengesi (NED) ile karşı karşıya kalmaktadır. Geçiş döneminde şekillenen metabolik bozukluklar diğer sekonder sağlık sorunlarının öncülü niteliğindedir. Laktasyonun ilk haftalarında besin maddesi arzı ile talebi arasındaki dengesizlik, metabolizmanın kapsamlı bir adaptasyon ve regülasyon sürecine girmesini zorunlu kılmaktadır. Metabolik profil (parametre) testleri; kan, serum veya sütteki serbest yağ asitleri, β-hidroksibütirik asit ve glukoz gibi metabolitler aracılığıyla hayvanın metabolik durumunun izlenmesine olanak tanır. Bu derlemede, geçiş dönemi metabolik göstergelerinin referans değerlerden sapmasının üreme parametreleri (doğum sonrası ilk kızgınlık, kızgınlık belirleme oranı, ilk tohumlama, ilk tohumlamada gebelik oranı, gebelik başına tohumlama sayısı) ve metabolik hastalıklar (ketozis, süt humması, plasentanın atılamaması, metritis, abomasum yer değiştirmesi ve topallık) üzerindeki etkileri güncel literatür ışığında incelenmiştir. Ayrıca, enerji metabolizmasının önemi, patolojik süreçler ve üreme ile olan etkileşimleri ve saha koşullarında sürü izleme stratejileri ele alınmıştır. Sonuç olarak; geçiş döneminde metabolik profil testleri ile yapılan düzenli izlemeler, olası metabolik bozuklukların erken teşhis edilmesini sağlayarak sürü sağlığı ve üreme başarısının korunmasında kilit rol oynamaktadır. Elde edilen veriler ışığında, geçiş dönemindeki homeoretik adaptasyonların ve metabolik göstergelerin doğru analiz edilmesinin, yüksek verimli süt sığırı işletmelerinde ekonomik kayıpların minimize edilmesine temel teşkil ettiği sonucuna varılmıştır.

Keywords

• sığır
• kuru dönem
• erken laktasyon
• negatif enerji dengesi
• metabolik durum
• döl verimi

Relationships Between Transition Period Metabolic Profile, Reproductive Performance, and Metabolic Disorders in Dairy Cattle

Abstract

The lactation cycle in dairy cows involves significant physiological, nutritional, metabolic, and immunological changes as it transitions from the final stage of pregnancy to the onset of high milk synthesis and secretion. The transition period, spanning the three weeks before calving and the three to four weeks after, is the most critical phase, as it determines milk yield, overall health status, and reproductive performance. During this period, cows face a negative energy balance (NED) due to increased energy requirements and decreased dry matter intake. Metabolic disorders that develop during the transition are precursors to other secondary health issues. The imbalance between nutrient supply and demand in the first weeks of lactation necessitates comprehensive metabolic adaptation and regulation processes. Metabolic profile (parameter) tests, through metabolites such as free fatty acids, ß-hydroxybutyric acid, and glucose in blood, serum, or milk, enable monitoring of the animal's metabolic status. This review examines, in light of current literature, how deviations from reference values in metabolic indicators during the transition period affect reproductive parameters (e.g. the first postpartum estrus, estrus detection rate, first insemination, pregnancy rate at first insemination, and number of inseminations per pregnancy) and metabolic diseases (ketosis, milk fever, retained placenta, metritis, displaced abomasum, and lameness). Additionally, the importance of energy metabolism, pathological processes, their interactions with reproduction, and herd-monitoring strategies in field conditions is discussed. In conclusion, regular monitoring of metabolic profiles during the transition period is key to early detection of potential metabolic disorders, thereby safeguarding herd health and reproductive success. Based on the data obtained, it is concluded that an accurate analysis of homeorhetic adaptations and metabolic indicators during the transition period is essential for minimising economic losses in high-yield dairy operations.

Keywords

• cattle
• dry period
• early lactation
• negative energy balance
• metabolic state
• fertility

References

1. Altaş, T., Yıldırım, R., 2023. Süt ineklerinde propilen glikol ve gliserol kullanımının betahidroksibutirik asit, esterleşmemiş yağ asitleri ve vücut kondisyon skoru üzerine etkileri. Journal of Research in Veterinary Medicine. 42(1), 48-54.https://doi.org/ 10.30782/jrvm.1224380
2. Arslan, C., Tufan, T., 2010. Geçiş dönemindeki süt ineklerinin beslenmesi II: Bu dönemde görülen metabolik hastalıklar ve besleme ile önlenmesi. Kafkas Üniversitesi Veteriner Fakültesi Dergisi. 16(1): 159–166. https://doi.org/10.9775/kvfd.2009.443
3. Ashar, M. J., Gonzalez-Rivas, P. A., Dunshea, F. R., Marth, C. D., Chauhan, S. S., 2026. Integrative ınsights into metabolic, oxidative, and ımmune adaptations during the transition period in dairy cows: revisiting nutritional strategies and emerging roles of ınjectable trace minerals. Dairy, 7(1), 15. https://doi.org/10.3390/dairy7010015
4. Bell, A.W., 1995. Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. Journal of Animal Science. 73: 2804–2819.
5. Berge, A. C., Vertenten, G., 2014. A field study to determine the prevalence, dairy herd management systems, and fresh cow clinical conditions associated with ketosis in western European dairy herds. Journal of Dairy Science. 97(4): 2145-2154. https://doi.org/10.3168/jds.2013-7163
6. Bobe, G., Young, J. W., Beitz, D. C., 2004. Invited review: pathology, etiology, prevention, and treatment of fatty liver in dairy cows. Journal of Dairy Science. 87(10): 3105-3124.
7. Borş, S. I., Solcan, G., Vlad-Sabie, A., 2014. Effects of propylene glycol supplementation on blood indicators of hepatic function, body condition score, milk fat-protein concentration and reproductive performance of dairy cows. Acta Veterinaria Brno. 83(1): 27-32. https://doi.org/10.2754/avb201483010027
8. Burfeind, O., Heuwieser, W., 2012. Validation of handheld meters to measure blood L-lactate concentration in dairy cows and calves. Journal of Dairy Science. 95(11): 6449-6456. https://doi.org/10.3168/jds.2012-5329

9. Butler, W. R., 2003. Energy balance relationships with follicular development ovulation and fertility in postpartum dairy cows. Livestock Production Science. 83, 211-218.
10. Butler, S. T., Marr, A. L., Pelton, S. H., Radcliff, R. P., Lucy, M. C., Butler. W. R., 2003. Insulin restores GH responsiveness during lactation-induced negative energy balance in dairy cattle: Effects on expression of IGF-I and GH receptor 1A. Journal of Endocrinology. 176:205–217.
11. Ceciliani, F., Ceron, J. J., Eckersall, P. D., Sauerwein, H., 2012. Acute phase proteins in ruminants. Journal of Proteomics. 75(14): 4207-4231. https://doi.org/10.1016/ j.jprot.2012.04.004
12. Carvalho, P. D., Souza, A. H., Amundson, M. C., Hackbart, K. S., Fuenzalida, M. J., Herlihy, M. M., Ayres, M. M., Ayres, H. D., Dresch, A. R., Vieira, L. M., Guenther, R. R., Grummer, R. R., Fricke, P. M., Shaver, R. D., Wiltbank. M. C., 2014. Relationships between fertility and post-partum changes in body condition and body weight in lactating dairy cows. Journal of Dairy Science. 97:3666–3683. https: //doi.org/10.3168/jds.2013-7809.
13. Caixeta, L. S., Omontese, B. O., 2021. Monitoring and improving the metabolic health of dairy cows during the transition period. Animals. 11(2): 352. https://doi.org/10.3390/ ani11020352
14. Cheng, Z., McLaughlin, D.L., Little, M.W., Ferris, C., Salavati, M., Ingvartsen, K. L., Crowe, M. A., Wathes, D. C., 2023. Proportion of concentrate in the diet of early lactation dairy cows has contrasting effects on circulating leukocyte global transcriptomic profiles, health and fertility according to parity. International Journal of Molecular Sciences. 24(1): 39. https://doi.org/10.3390/ijms24010039
15. Chirivi, M., Cortes-Beltran, D., Munsterman, A., O'Connor, A., Contreras, G. A., 2023. Lipolysis inhibition as a treatment of clinical ketosis in dairy cows: A randomized clinical trial. Journal of Dairy Science. 106(12), 9514-9531. https://doi.org/ 10.3168/jds.2023-23409
16. Contreras, G. A., Strieder-Barboza, C., Raphael, W., 2017. Adipose tissue lipolysis and remodeling during the transition period of dairy cows. Journal of Animal Science and Biotechnology. 8(1): 41. https://doi.org/10.1186/s40104-017-0174-4
17. Dağdelen, K., Alan, B. S., Camgöz, A., Altunok, V., 2022. Süt ineği yetiştiriciliğinde kan metabolik profili testleri. Veteriner Farmakoloji ve Toksikoloji Derneği Bülteni. 13(3): 152-162. https://doi.org/10.38137/vftd.1177485
18. Dann, H. M., Litherland, N. B., Underwood, J. B., Bionaz, M., Dangelo, M., McFadden, J. W., Drackley, J. K., 2006. Diets during far-off and close-up dry periods affect periparturient metabolism and lactation in multiparous cows. Journal of Dairy Science. 89 (9): 3563-3577.
19. Dervishi, E., Plastow, G., Hoff, B., & Colazo, M. (2021). Common and specific mineral and metabolic features in dairy cows with clinical metritis, hypocalcaemia or ketosis. Research in Veterinary Science. 135, 335-342. https://doi.org/10.1016/ j.rvsc.2020.10.012
20. Drackley, J.K., Overton, T.R., Douglas, G.N., 2001. Adaptations of glucose and long-chain fatty acid metabolism in liver of dairy cows during the periparturient period. Journal of Dairy Science. 84 (Suppl.): E100-E112 https://doi.org/10.3168/jds.S0022-0302(01)70204-4
21. Ehrhardt, R. A., Slepetis, R. M., Siegel-Willott, J., Van Amburgh, M. E., Bell, A. W., Boisclair, Y. R., 2000. Development of a specific radioimmunoassay to measure physiological changes of circulating leptin in cattle and sheep. Journal of Endocrinology. 166(3): 519-528.
22. Esposito, G., Irons, P. C., Webb, E. C., Chapwanya, A., 2014. Interactions between negative energy balance, metabolic diseases, uterine health and immune response in transition dairy cows. Animal Reproduction Science. 144(3-4): 60-71. https://doi.org/10.1016/ j.anireprosci.2013.11.007
23. Giannuzzi, D., Mota, L. F. M., Schiavon, S., Gallo, L., Pegolo, S., Ajmone Marsan, P., Tagliapietra, F., Trevisi, E., Cecchinato, A., 2023. Prediction of detailed blood metabolic profile using milk infrared spectra and machine learning methods in dairy cattle. Journal of Dairy Science. 106(5): 3321–3344. https://doi.org/10.3168/jds.2022-22454
24. Gobikrushantha, M., Macmillan, K., Behrouzi, A., López-Helguera, I., Hoff, B., Colazo, M. G., 2020. Circulating Ca and its relationship with serum minerals, metabolic and nutritional profiles, health disorders, and productive and reproductive outcomes in dairy cows. Livestock Science. 233: 103946. https://doi.org/10.1016/j.livsci.2020.103946
25. Goff, J. P., 2008. The monitoring, prevention, and treatment of milk fever and subclinical hypocalcemia in dairy cows. Vet J. 2008;176(1):50–7.
26. Grummer, R.R., 1995. Impact of changes in organic nutrient metabolism on feeding the transition dairy cow. Journal of Animal Science. 73: 2820–2833.
27. Hammon, H. M., Stürmer, G., Schneider, F., Tuchscherer, A., Blum, H., Engelhard, T., Genzel, A., Staufenbiel, R., Kanitz, W. L., 2009. Performance and metabolic and endocrine changes with emphasis on glucose metabolism in high-yielding dairy cows with high and low fat content in liver after calving. Journal of Dairy Science. 92(4): 1554-1566. https://doi.org/ 10.3168/jds.2008-1634
28. Hayirli, A., Grummer, R. R., Nordheim, E. V., Crump, P. M., 2002. Animal and dietary factors affecting feed intake during the prefresh transition period in Holsteins. Journal of Dairy Science. 85(12): 3430-3443. https://doi.org/10.3168/jds.S0022-0302(02)74431-7
29. Hildebrand, C., Hollenbach, J., Seeger, B., Pfarrer, C., 2023. ß-hydroxybutyrate effects on bovine caruncular epithelial cells: A model for ınvestigating the peri-ımplantation period disruption in ketotic dairy cows. Animals. 13(18): 2950. https://doi.org/10.3390/ ani13182950
30. Horst, E. A., Kvidera, S. K., Baumgard, L. H., 2021. Invited review: The influence of immune activation on transition cow health and performance – A critical evaluation of traditional dogmas. Journal of Dairy Science. 104(8): 8380-8410. https://doi.org/10.3168 /jds.2021-20330
31. Ingvartsen, K. L., Boisclair, Y. R., 2001. Leptin and the regulation of food intake, energy homeostasis and immunity with special focus on periparturient ruminants. Domestic Animal Endocrinology. 21(4): 215-250.
32. Jeong, J. K., Choi, I. S., Kang, H. G., Hur, T. Y., Jung, Y. H., Kim, I. H., 2015. Relationship between serum metabolites, body condition, peri-and postpartum health and resumption of postpartum cyclicity in dairy cows. Livestock Science. 181: 31-37. https://doi.org/ 10.1016/j.livsci.2015.09.022
33. Kabir, M., Hasan, M. M., Tanni, N. S., Parvin, M. S., Asaduzzaman, M., Ehsan, M. A., Islam, M. T., 2022. Metabolic profiling in periparturient dairy cows and its relation with metabolic diseases. BMC Research Notes. 15(1): 231. https://doi.org/10.1186/s13104-022-06130-z
34. Kayano, M., Kida, K., 2015. Identifying alterations in metabolic profiles of dairy cows over the past two decades in Japan using principal component analysis. Journal of Dairy Science. 98(12): 8764-8774. https://doi.org/10.3168/jds.2015-9791
35. Kwon, E. G., Cho, Y. M., Choi, Y. H., Park, B. K., Chung, H. J., Choi, N. J., Ahn, B. S., Kim, J. B., 2006. Effects of maternal genetic potential and parity with pre- and postpartum on body weights, body condition score and blood metabolites in Hanwoo cows. Journal of Animal Science and Technology. 48: 881-888. https://doi.org/10.5187/ JAST.2006.48.6.881
36. LeBlanc, S., 2010. Monitoring metabolic health of dairy cattle in the transition period. Journal of Reproduction and Development. 56(S): S29-S35. https://doi.org/10.1262/ jrd.1056S29
37. Liefers, S. C., Veerkamp, R. F., Te Pas, M. F. W., Delavaud, C., Chilliard, Y., Van der Lende, T., 2003. Leptin concentrations in relation to energy balance, milk yield, intake, live weight, and estrus in dairy cows. Journal of Dairy Science. 86(3): 799-807. https://doi.org/10.3168/jds.S0022-0302(03)73662-5
38. Leroy, J. L., M. R., Opsomer, G., Van Soom, A., Goovaerts, I. G. F., Bols, P. E. J., 2008. Reduced fertility in high-yielding dairy cows: Are the oocyte and embryo in danger? Part I. The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high-yielding dairy cows. Reproduction in Domestic Animals. 43:612–622. https: //doi.org/10.1111/j.1439-0531.2007.00960.x
39. Leroy, J. L. M. R., Vanholder, T. B., Mateusen, A., Christophe, G., Opsomer, A., de Kruif, G., Genicot, A., Van Soom, A., 2005. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130(4):485–495. https://doi.org/10.1530/rep.1.00735
40. Lucy, M. C., Jiang, H.,Kobayashi,Y.,2001. Changes in the somatotrophic axis associated with the initiation of lactation. Journal of Dairy Science. 84(E Suppl.):E113–E119.
41. Macrae, A. I., Whitaker, D. A., Burrough, E., Dowell, A., Kelly, J. M., 2006. Use of metabolic profiles for the assessment of dietary adequacy in UK dairy herds. Veterinary Record. 159(20): 655-661.
42. Martens, H. (2023). Invited review: increasing milk yield and negative energy balance: a gordian knot for dairy cows?. Animals. 13(19): 3097. https://doi.org/10.3390/ ani13193097
43. McArt, J. A. A., Nydam, D. V., Oetzel, G. R., 2012. Epidemiology of subclinical ketosis in early lactation dairy cattle. Journal of Dairy Science. 95(9): 5056-5066. https://doi.org/10.3168/jds.2012-5443
44. McArt, J. A., Nydam, D. V., Oetzel, G. R., Overton, T. R., Ospina, P. A., 2013. Elevated non-esterified fatty acids and β-hydroxybutyrate and their association with transition dairy cow performance. The Veterinary Journal. 198(3): 560-570. https://doi.org/10.1016/ j.tvjl.2013.08.011
45. McArt, J. A. A., Nydam, D. V., Overton, M. W., 2015. Hyperketonemia in early lactation dairy cattle: A deterministic estimate of component and total cost per case. Journal of Dairy Science. 98(3), 2043-2054. https://doi.org/10.3168/jds.2014-8740
46. McGuffey, R. K., 2017. A 100-Year Review: Metabolic modifiers in dairy cattle nutrition. Journal of Dairy Science. 100(12): 10113-10142. https://doi.org/10.3168/ jds.2017-12987
47. Melendez, P., Chelikani, P. K., 2022. Dietary cation-anion difference to prevent hypocalcemia with emphasis on over-acidification in prepartum dairy cows. Animal. 16(10), 100645. https://doi.org/10.1016/j.animal.2022.100645
48. Meral, Y., Kara, Ç., 2013. Geçiş dönemindeki süt sığırlarında karaciğer yağlanması ve kolinin önemi. Uludağ Üniversitesi Veteriner Fakültesi Dergisi. 32(1), 39-46.
49. Moghimi-Kandelousi, M., Alamouti, A. A., Imani, M., Zebeli, Q., 2020. A meta-analysis and meta-regression of the effects of vitamin E supplementation on serum enrichment, udder health, milk yield, and reproductive performance of transition cows. Journal of Dairy Science. 103(7): 6157-6166. https://doi.org/10.3168/jds.2019-17556
50. NASEM, 2021. National Academies of Sciences, Engineering, and Medicine. Nutrient Requirements of Dairy Cattle. 8th rev. ed. Washington DC: The National Academies Press. https://doi.org/10.17226/25806.
51. Ocak, N., Garipoğlu, A.V., 2023. Süt Sığırlarının Beslenmesi. In G. Erener, & A. Altop (Eds.), Hayvan Beslemede Güncel Yaklaşımlar-I (pp. 469-574). İstanbul, Türkiye: Efe Akademik Yayıncılık.
52. Ospina, P. A., Nydam, D. V., Stokol, T., Overton, T. R., 2010a. Evaluation of nonesterified fatty acids and β-hydroxybutyrate in transition dairy cattle in the northeastern United States: Critical thresholds for prediction of clinical diseases. Journal of Dairy Science. 93(2): 546-554.https://doi.org/10.3168/jds.2009-2277
53. Ospina, P. A., Nydam, D. V., Stokol, T., Overton, T. R., 2010b. Associations of elevated nonesterified fatty acids and β-hydroxybutyrate concentrations with early lactation reproductive performance and milk production in transition dairy cattle in the northeastern United States. Journal of Dairy Science. 93(4): 1596-1603. https://doi.org/ 10.3168/jds.2009-2852
54. Patton, J., Kenny, D. A., McNamara, S., Mee, J. F., O’Mara, F. P.,Diskin, M. G., Murphy,J. J., 2007. Relationships among milk production, energy balance, plasma analytes, and reproduction in Holstein-Friesian cows. Journal of Dairy Science. 90:649-658. https: //doi.org/10.3168/jds.S0022-0302(07)71547-3.
55. Payne, J. M., Dew, S. M., Manston, R., Faulks, M., 1970. The use of a metabolic profile test in dairy herds. Veterinary Record. 87:150-158.
56. Pascottini, O. B., Leroy, J. L., Opsomer, G., 2020. Metabolic stress in the transition period of dairy cows: Focusing on the prepartum period. Animals. 10(8): 1419. https://doi.org/ 10.3390/ani10081419
57. Pascottini, O. B., Leroy, J. L., Opsomer, G., 2022. Maladaptation to the transition period and consequences on fertility of dairy cows. Reproduction in Domestic Animals. 57: 21-32. https://doi.org/10.1111/rda.14176
58. Pushpakumara, P. G. A., Gardner, N. H., Reynolds, C. K., Beever, D. E., Wathes, D. C., 2003. Relationships between transition period diet, metabolic parameters and fertility in lactating dairy cows. Theriogenology. 60(6): 1165-1185.
59. Rhoads, M. L., Gilbert, R. O., Lucy, M. C., Butler, W. R., 2004. Effects of urea infusion on the uterine luminal environment of dairy cows. Journal of Dairy Science. 87(9): 2896-2901.
60. Rhoads, M. L., Meyer, J. P., Kolath, S. J., Lamberson, W. R., Lucy, M. C., 2008. Growth hormone receptor, insulin-like growth factor (IGF)-1, and IGF-binding protein-2 expression in the reproductive tissues of early postpartum dairy cows. Journal of Dairy Science. 91(5): 1802-1813. https://doi.org/10.3168/jds.2007-0664
61. Rhoads, M. L., Rhoads, R. P., Gilbert, R. O., Toole, R., Butler, W. R., 2006. Detrimental effects of high plasma urea nitrogen levels on viability of embryos from lactating dairy cows. Animal Reproduction Science. 91(1-2): 1-10.https://doi.org/10.1016/ j.anireprosci.2005.02.009
62. Roche, J. R., Kay, J. K., Friggens, N. C., Loor, J. J., Berry, D. P., 2013. Assessing and managing body condition score for the prevention of metabolic disease in dairy cows. Veterinary Clinics: Food Animal Practice. 29(2): 323-336.
63. Saavedra, L. P., Francisco, F. A., Raposo, S. R., Cavalcante, K. V., Buttow, N. C., Borges, S. C., Gomes, R. M., Campos, H. M., Gonçalves, G. D., Piovan, S., Ghedini, P. C., Prates, K. V., Malta, A., Matafome, P., Mathias, P. C. F., Almeida, D. L., 2025. Maternal age precursors during lactation alter offspring glycemic homeostasis early in life. Biology. 4(2): 160. https://doi.org/10.3390/ biology14020160
64. Santos, J. E. P., Lean, I. J., Golder, H., Block, E., 2019. Meta-analysis of the effects of prepartum dietary cation-anion difference on performance and health of dairy cows. Journal of Dairy Science. 102(3): 2134-2154. https://doi.org/10.3168/jds.2018-14628
65. Serbester, U., Çinar, M., Hayirli, A., 2012. Sütçü ineklerde negatif enerji dengesi ve metabolik indikatörleri. Kafkas Üniversitesi Veteriner Fakültesi Dergisi.18(4): 705-711.https://doi.org/10.9775/kvfd.2012.6559
66. Sevinç, M., Başoğlu, A., Güzelbektaş, H., Boydak, M., 2003. Lipid and lipoprotein levels in dairy cows with fatty liver. Turkish Journal of Veterinary & Animal Sciences. 27(2): 295-299.
67. Sordillo, L. M., Raphael, W., 2013. Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. Veterinary Clinics: Food Animal Practice. 29(2): 267-278.
68. Sun, L., Huang, J., Dou, X., Dong, Z., Li, Y., Tan, S., Yu, R., Li, C., Zhao, W., 2025. Resveratrol alleviates nefa-ınduced oxidative damage in bovine mammary epithelial cells by restoring mitochondrial function. Animals. 15(2): 118. https://doi.org/10.3390 /ani15020118
69. Suthar, V. S., Canelas-Raposo, J., Deniz, A., Heuwieser, W., 2013. Prevalence of subclinical ketosis and relationships with postpartum diseases in European dairy cows. Journal of Dairy Science. 96(5): 2925-2938. https://doi.org/10.3168/jds.2012-6035
70. Taylor, V. J., Cheng, Z., Pushpakumara, P. G. A., Beever, D. E., Wathes, D. C., 2004. Relationships between the plasma concentrations of insulin-like growth factor-I in dairy cows and their fertility and milk yield. Veterinary Record. 155:583–588.
71. Tufarelli, V., Puvača, N., Glamočić, D., Pugliese, G., Colonna, M. A., 2024. The most important metabolic diseases in dairy cattle during the transition period. Animals. 14(5): 816. https://doi.org/10.3390/ani14050816
72. Westwood, C. T., Lean, I. J., Garvin, J. K., 2002. Factors influencing fertility of Holstein dairy cows: a multivariate description. Journal of Dairy Science. 85:3225-3237.
73. Wankhade, P.R., Manimaran, A., Kumaresan, A., Jeyakumar, S., Ramesha, K.P., Sejian, V., Rajendran, D., Varghese, M. R., 2017. Metabolic and immunological changes in transition dairy cows: A review, Veterinary World. 10(11): 1367-1377. https: //doi.org/10.14202/ vetworld.2017.1367-1377
74. Wathes, D. C., 2012. Mechanisms linking metabolic status and disease with reproductive outcome in the dairy cow. Reproduction in Domestic Animals. 47:304–312. https: //doi.org/10.1111/j.1439-0531.2012.02090.x.
75. Wathes, D. C., Becker, F., Buggiotti, L., Crowe, M. A., Ferris, C., Foldager, L., Grelet, C., Hostens, M., Ingvartsen, Klaus L., Marchitelli, C., Salavati, M., Signorelli, F., Takeda, H., Tang, L., Cheng Z., the GplusE Consortium, 2021. Associations between circulating IGF-1 concentrations, disease status and the leukocyte transcriptome in early lactation dairy cows. Ruminants. 1(2): 147-177. https://doi.org/10.3390/ruminants1020012
76. Wathes, D. C., Cheng, Z., Bourne, N., Taylor, V. J., Coffey, M. P., Brotherstone, S., 2007. Differences between primiparous and multiparous dairy cows in the inter-relationships between metabolic traits, milk yield and body condition score in the periparturient period. Domestic Animal Endocrinology. 33(2): 203-225.
77. Yılmaz, Ö., Rişvanlı, A., 2021. İneklerde postpartum dönemdeki hastalıklarda sitokin düzeyleri. Erciyes Üniversitesi Veteriner Fakültesi Dergisi. 18(2): 116-121. https://doi.org/10.32707/ercivet.953201
78. Zarrin, M., De Matteis, L., Vernay, M. C. M. B., Wellnitz, O., van Dorland, H. A., Bruckmaier, R. M., 2013. Long-term elevation of β-hydroxybutyrate in dairy cows through infusion: Effects on feed intake, milk production, and metabolism. Journal of Dairy Science. 96(5): 2960-2972. https://doi.org/10.3168/jds.2012-6224
79. Zhao, X., Zheng, N., Zhang, Y., Wang, J., 2025. The role of milk urea nitrogen in nutritional assessment and its relationship with phenotype of dairy cows: A review. Animal Nutrition. 20: 33-41. https://doi.org/10.1016/j.aninu.2024.08.007
80. Zhang, Z., Liu, G., Li, X., Wang, Z., Kong, T., Zhang, N., Guo, C., 2009. Beta-hydroxybutyrate, glucose, calcium, phosphorus, and vitamin C concentrations in blood of dairy cows with subclinical ketosis during the early lactation. Bulletin of the Veterinary Institute in Puławy. 53(1): 71-74.