{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,20]],"date-time":"2026-01-20T11:40:32Z","timestamp":1768909232574,"version":"3.49.0"},"reference-count":43,"publisher":"MDPI AG","issue":"20","license":[{"start":{"date-parts":[[2024,10,21]],"date-time":"2024-10-21T00:00:00Z","timestamp":1729468800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>A suboptimal intrauterine environment during gestation may result in the programming of long-lasting structural and physiological alterations in the developing fetus, leading to health and production complications in adulthood. This observational study aimed to identify the impact of exposure to the summer season at different trimesters of gestation, dam parity, and their interaction on the postpartum disease incidence, first-lactation milk production, and herd lifespan of the offspring (F1 generation). Using a dataset collected from two commercial herds, the female offspring were categorized into three groups based on the trimester their dams experienced summer season during pregnancy: (1) first trimester (n = 2345), (2) second trimester (n = 3513), and (3) final trimester (n = 4988). The estimated 305-day milk production was lower in daughters (as a first-lactation cow) born to dams exposed to summer season during the first vs. third trimester. Summer season exposure during the first vs. third trimester resulted in the offspring that were less likely to remain in the herd (hazard ratio = 0.90; 95% CI = 0.84\u20130.95). Daughters of parous vs. nulliparous dams were more likely to experience dystocia and metritis but less likely to experience retained placenta. The risk of culling was higher in daughters of parous vs. nulliparous dams. Our preliminary findings suggest that the first trimester is a critical determinant of the female progeny\u2019s future productive performance and survivability. Dam parity was also identified as an influential factor affecting offspring health, as dystocia and metritis were more prevalent, and the culling risk was greater in daughters born to parous dams.<\/jats:p>","DOI":"10.3390\/ani14203040","type":"journal-article","created":{"date-parts":[[2024,10,21]],"date-time":"2024-10-21T08:53:11Z","timestamp":1729500791000},"page":"3040","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Does Exposure to Summer Season at Different Stages of Intrauterine Development and Maternal Parity Affect Health and First-Lactation Milk Production of Female Offspring of Holstein Cows?"],"prefix":"10.3390","volume":"14","author":[{"given":"Hamed","family":"Beiranvand","sequence":"first","affiliation":[{"name":"R&D Department of Chaltasian & Talise Asil Jahan Agro-Animal Husbandry, Varamin 33751-13111, Iran"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Abolfazl","family":"Mahnani","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences, College of Agriculture, Isfahan University of Technology, Isfahan 84156-83111, Iran"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5453-1083","authenticated-orcid":false,"given":"Ali","family":"Kahyani","sequence":"additional","affiliation":[{"name":"Department of Animal Science, School of Agriculture, Shiraz University, Shiraz 71441-65186, Iran"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3998-1240","authenticated-orcid":false,"given":"Frank R.","family":"Dunshea","sequence":"additional","affiliation":[{"name":"School of Agriculture, Food and Ecosystem Sciences, Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"},{"name":"Faculty of Biological Sciences, The University of Leeds, Leeds LS2 9JT, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Farhad","family":"Ahmadi","sequence":"additional","affiliation":[{"name":"School of Agriculture, Food and Ecosystem Sciences, Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,10,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1071\/RD16410","article-title":"Epidemiological evidence for metabolic programming in dairy cattle","volume":"29","author":"Opsomer","year":"2017","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e51816","DOI":"10.1371\/journal.pone.0051816","article-title":"Trans-generational effect of maternal lactation during pregnancy: A Holstein cow model","volume":"7","author":"Ugarte","year":"2012","journal-title":"PLoS ONE"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"6631","DOI":"10.3168\/jds.2017-12662","article-title":"Season of conception is associated with future survival, fertility, and milk yield of Holstein cows","volume":"100","author":"Pinedo","year":"2017","journal-title":"J. Dairy Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"49","DOI":"10.3389\/fgene.2013.00049","article-title":"Maternal diet during pregnancy induces gene expression and DNA methylation changes in fetal tissues in sheep","volume":"4","author":"Lan","year":"2013","journal-title":"Front. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1079\/PNS2005478","article-title":"Developmental programming of health and disease","volume":"65","year":"2006","journal-title":"Proc. Nutr. Soc."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2316","DOI":"10.2527\/jas.2006-156","article-title":"Board-invited review: Intrauterine growth retardation: Implications for the animal sciences","volume":"84","author":"Wu","year":"2006","journal-title":"J. Anim. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"8443","DOI":"10.3168\/jds.2016-11072","article-title":"In utero heat stress decreases calf survival and performance through the first lactation","volume":"99","author":"Monteiro","year":"2016","journal-title":"J. Dairy Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1146\/annurev-animal-031412-103644","article-title":"Effects of heat stress on postabsorptive metabolism and energetics","volume":"1","author":"Baumgard","year":"2013","journal-title":"Annu. Rev. Anim. Biosci."},{"key":"ref_9","unstructured":"IPCC (2022). Climate Change: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, IPCC."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"8645","DOI":"10.3168\/jds.2017-12651","article-title":"Invited review: Effects of heat stress on dairy cattle welfare","volume":"100","author":"Polsky","year":"2017","journal-title":"J. Dairy Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"4079","DOI":"10.3168\/jds.2012-6278","article-title":"Invited review: Heat stress effects during late gestation on dry cows and their calves","volume":"96","author":"Tao","year":"2013","journal-title":"J. Dairy Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1093\/af\/vfab059","article-title":"Consequences of maternal heat stress at different stages of embryonic and fetal development on dairy cows\u2019 progeny","volume":"11","author":"Ouellet","year":"2021","journal-title":"Anim. Front."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1113\/jphysiol.2005.104430","article-title":"Evidence for altered placental blood flow and vascularity in compromised pregnancies","volume":"572","author":"Reynolds","year":"2006","journal-title":"J. Physiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"7555","DOI":"10.3168\/jds.2020-18154","article-title":"Late-gestation heat stress impairs daughter and granddaughter lifetime performance","volume":"103","author":"Laporta","year":"2020","journal-title":"J. Dairy Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"skac399","DOI":"10.1093\/jas\/skac399","article-title":"Dam parity affects fetal growth, placental size, and neonatal metabolism in spring-born beef calves","volume":"101","author":"Duncan","year":"2023","journal-title":"J. Anim. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.theriogenology.2023.07.012","article-title":"Developmental programming of production and reproduction in dairy cows: I. Association of maternal parity with offspring\u2019s birth weight, milk yield, reproductive performance and AMH concentration during the first lactation period","volume":"210","author":"Bafandeh","year":"2023","journal-title":"Theriogenology"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Wathes, D.C. (2022). Developmental programming of fertility in cattle\u2014Is it a cause for concern?. Animals, 12.","DOI":"10.3390\/ani12192654"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1379","DOI":"10.1016\/j.theriogenology.2007.02.009","article-title":"Climate factors affecting conception rate of high producing dairy cows in northeastern Spain","volume":"67","author":"Santolaria","year":"2007","journal-title":"Theriogenology"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1338","DOI":"10.1002\/vms3.1088","article-title":"Effects of fresh-cow grouping strategy and rumen-protected glucose on production performance, reproductive variables and risk of culling in Holstein cows","volume":"9","author":"Beiranvand","year":"2023","journal-title":"Vet. Med. Sci."},{"key":"ref_20","unstructured":"National Research Council (NRC) (2001). Nutritional Requirements of Dairy Cattle, National Academies Press. [7th ed.]."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1016\/S0093-691X(99)00275-7","article-title":"Effects of severity of dystocia on cold tolerance and serum concentrations of glucose and cortisol in neonatal beef calves","volume":"53","author":"Bellows","year":"2000","journal-title":"Theriogenology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1693","DOI":"10.3168\/jds.S0022-0302(95)76794-7","article-title":"The association between previous 305-day milk yield and disease in New York State dairy cows","volume":"78","author":"Eicker","year":"1995","journal-title":"J. Dairy Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1516","DOI":"10.1016\/j.theriogenology.2005.08.021","article-title":"Defining postpartum uterine disease in cattle","volume":"65","author":"Sheldon","year":"2006","journal-title":"Theriogenology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4232","DOI":"10.3168\/jds.2022-22394","article-title":"Estimation of body condition score change in dairy cows in a seasonal calving pasture-based system using routinely available milk mid-infrared spectra and machine learning techniques","volume":"106","author":"Frizzarin","year":"2023","journal-title":"J. Dairy Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.theriogenology.2023.09.002","article-title":"Developmental programming of production and reproduction in dairy cows: II. Association of gestational stage of maternal exposure to heat stress with offspring\u2019s birth weight, milk yield, reproductive performance and AMH concentration during the first lactation period","volume":"212","author":"Makiabadi","year":"2023","journal-title":"Theriogenology"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1514","DOI":"10.3168\/jds.S0022-0302(80)83111-0","article-title":"Partitioning of nutrients during pregnancy and lactation: A review of mechanisms involving homeostasis and homeorhesis","volume":"63","author":"Bauman","year":"1980","journal-title":"J. Dairy Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1016\/j.semcdb.2012.03.018","article-title":"Growth and development of the mammary glands of livestock: A veritable barnyard of opportunities","volume":"23","author":"Rowson","year":"2012","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_28","unstructured":"Akers, R.M. (2002). Lactation and the Mammary Gland, Blackwell Publishing Co.. [1st ed.]."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"810","DOI":"10.1002\/mrd.23040","article-title":"Cellular and epigenetic changes induced by heat stress in bovine preimplantation embryos","volume":"85","year":"2018","journal-title":"Mol. Reprod. Dev."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Kasimanickam, R., and Kasimanickam, V. (2021). Impact of heat stress on embryonic development during first 16 days of gestation in dairy cows. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-94278-2"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1477-7827-11-3","article-title":"Changes in the transcriptome of morula-stage bovine embryos caused by heat shock: Relationship to developmental acquisition of thermotolerance","volume":"11","author":"Sakatani","year":"2013","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Mi\u0119tkiewska, K., Kordowitzki, P., and Pareek, C.S. (2022). Effects of heat stress on bovine oocytes and early embryonic development\u2014An update. Cells, 11.","DOI":"10.3390\/cells11244073"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1016\/0093-691X(92)90155-K","article-title":"Factors affecting calf birth weight: A review","volume":"38","author":"Holland","year":"1992","journal-title":"Theriogenology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.placenta.2005.12.002","article-title":"Nutritional modulation of adolescent pregnancy outcome\u2014A review","volume":"27","author":"Wallace","year":"2006","journal-title":"Placenta"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"823","DOI":"10.3168\/jds.2019-17083","article-title":"Associations between maternal characteristics and health, survival, and performance of dairy heifers from birth through first lactation","volume":"103","author":"Carvalho","year":"2020","journal-title":"J. Dairy Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2357","DOI":"10.1113\/jphysiol.2014.271460","article-title":"The biology of developmental plasticity and the Predictive Adaptive Response hypothesis","volume":"592","author":"Bateson","year":"2014","journal-title":"J. Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1017\/S2040174415001105","article-title":"Embryos, DOHaD and David Barker","volume":"6","author":"Fleming","year":"2015","journal-title":"J. Dev. Orig. Health Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1111\/j.1740-8709.2005.00020.x","article-title":"The developmental origins of adult disease","volume":"1","author":"Gluckman","year":"2005","journal-title":"Matern. Child Nutr."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1002\/mrd.22635","article-title":"Cellular and molecular mechanisms involved in placental separation in the bovine: A review","volume":"83","author":"Attupuram","year":"2016","journal-title":"Mol. Reprod. Dev."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2293","DOI":"10.3168\/jds.S0022-0302(04)70050-8","article-title":"Effect of maternal age on milk production traits, fertility, and longevity in cattle","volume":"87","author":"Reichl","year":"2004","journal-title":"J. Dairy Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"10251","DOI":"10.3168\/jds.2017-12968","article-title":"A 100-Year Review: Identification and genetic selection of economically important traits in dairy cattle","volume":"100","author":"Miglior","year":"2017","journal-title":"J. Dairy Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1710","DOI":"10.1093\/tas\/txz063","article-title":"The effect of dam age on heifer progeny performance and longevity","volume":"3","author":"Beard","year":"2019","journal-title":"Transl. Anim. Sci."},{"key":"ref_43","unstructured":"Beiranvand, H., Mahnani, A., Kahyani, A., Dunshea, F.R., and Ahmadi, F. (2024, January 8\u201312). Effects of summer season exposure at different trimesters of gestation on survival and first-lactation milk production capacity of the offspring. Proceedings of the Joint Asian-Australasian Association of Animal Production (AAAP) and Australian Association of Animal Science (AAAS) Animal Production Congress, Melbourne, Australia."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/14\/20\/3040\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:17:25Z","timestamp":1760113045000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/14\/20\/3040"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,21]]},"references-count":43,"journal-issue":{"issue":"20","published-online":{"date-parts":[[2024,10]]}},"alternative-id":["ani14203040"],"URL":"https:\/\/doi.org\/10.3390\/ani14203040","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,21]]}}}